CHAPTER 15

The pyramidal tract

HIROSHI ASANUMA The Rockefeller University, New York, New York

CHAPTER CONTENTS "sensory" cortex (areas 1, 2, and 3) as well as from

Organization of Projection From Cerebral Cortex to Spinal Cord
Studies by cortical surface stimulation
Studies by cortical depth stimulation
Microstructure of corticospinal projection
Projection to y-motoneurons
Projections to spinal intemeurons
Pyramidal collaterals and branches within brain
Afferent Inputs to Motor Cortex and Pyramidal Tract Neurons
General problems
Inputs from nucleus ventralis lateralis of thalamus
Peripheral inputs to motor cortex and pyramidal tract cells
Pathways from periphery to motor cortex
Functional significance of peripheral inputs to motor cortex
Inputs through association fibers
Inputs from sensory cortex
Inputs from association cortex
Inputs through commisural fibers
Function of Pyramidal Tract
Summary
THE PYRAMIDAL TRACT is by definition made up of all
those fibers that course longitudinally in the pyramids
of the medulla oblongata, regardless of their site of
origin or termination. These fibers are thought to
originate from cell bodies in the cerebral cortex, and
most of them continue into the spinal cord to consti-
tute the corticospinal tract. Some pyramidal tract
fibers leave the tract in the medulla and terminate at
cranial nerve nuclei in the brain stem. The existence
of the pyramidal fiber bundle had been known for a
long time, but the importance of this tract was grad-
ually recognized after the discovery of localization of
motor function within the cerebral cortex by Fritsch
and Hitzig in 1870 (53). After the introduction of the
Marchi method around 1880 (25), the origin and the
course of the pyramidal tract fibers were studied ex-
tensively. As early as 1889 Sherrington observed that
after lesion of the leg or arm area of the "motor"
co~ex in monkeys and dogs, the number of degener-
atmg fibers markedly diminished at the lower portions
of the lumbar or cervical enlargment, respectively ORGANIZATION OF PROJECTION FROM
(135, 136). After repeated experiments by a number of CEREBRAL CORTEX TO SPINAL CORD
investigators using this method, it became clear that
although the majority of the fibers originate from the Studies by Cortical Surface Stimulation
classic motor cortex (or area 4 of Brodmann) a con-
siderable fraction of them arise from the ~rimary After the discovery in 1870 of a motor representation
703
regions located anterior to the motor cortex (e.g., area
6). Details of the distribution of cells of origin of the
corticospinal tract are described in the chapter by
Kuypers in this Handbook.
Studies carried out by the Marchi method left many
unanswered questions, because this method necessi-
tates relatively large lesions in the cortex and stains
only degenerating myelinated fibers. The pyramidal
tract, however, contains a large number of nonmyeli-
nated or thinly myelinated fibers, and myelinated
fibers lose their myelin sheath at their terminal
branches. The use of the Nauta method (118) to trace
unmyelinated as well as the terminal branches of
degenerating fibers revealed finer details of pyramidal
tract organization. At about the same time, advances
in electrical recording techniques made it possible to
trace single as well as groups of pyramidal tract fibers
electroanatomically. Furthermore the recent develop-
ment of the horseradish peroxidase technique has
made it possible to determine the origin of neurons
projecting to limited areas in the spinal cord. As a
result of the application of these techniques, our
knowledge of the structure and function of the pyra-
midal tract system is growing rapidly. The interpre-
tation of the results, however, needs to be done care-
fully because the structure and possibly the function
of the pyramidal tract vary with the species studied.
For example, in carnivores all or nearly all of the
pyramidal tract fibers terminate on spinal intemeu-
rons (98), whereas in primates (22) and rodents (39)
some terminate directly on motoneurons. Because
most of the relevant experiments have been performed
using cats and monkeys, results with these animals are
emphasized. The description of the experiments is
limited in this chapter; therefore readers interested in
the details should refer to the original reports. Some
of the excellent reviews published recently are listed
in GENERAL REFERENCES.
704 HANDBOOK OF PHYSIOLOGY - THE NERVOUS SYSTEM II

in the cerebral cortex by Fritsch and Hitzig (53),
attempts were made to define the location of the
motor cortex using electrical current. As early as 1875
Ferrier (45) was able to draw a remarkably detailed
"motor map" (using faradic current instead of galvanic
current, as used earlier by Fritsch and Hitzig), al-
though this map included precentral, parietal, and also
temporal lobes (Fig. 1A). As time went on the methods
of stimulation and anesthesia were progressively im-
proved, so that by the turn of the century the area
representing motor function had shrunk to roughly
that seen in current textbooks (Fig. IB). During this
early stage of investigation, it was frequently asked
whether the structural organization of the motor cor-
tex is in accord with Hughlings Jackson's idea of
"minute representation." Strongly influenced by his
contemporary evolutionists, Jackson proposed that
the central nervous system is organized in a hierarchi-
cal fashion, i.e., the cerebral cortex controls the least
automatic movements, whereas automatic movements
are controlled by lower levels. According to this theory
there is widespread overlap in the representation of
muscles within the motor cortex. Each muscle would
be represented repeatedly in various parts ofthe motor
cortex, and a group of corticofugal neurons located in
a small area of the cortex would project to various
motor nuclei at several levels of the spinal cord. Hence
stimulation of a small area of the cortex would produce
contraction of a group of muscles (158). During the
course of his study with the chimpanzee and gorilla,
Sherrington (137) noted that the effect produced by
cortical stimulation was always coordinated contrac-
tion of muscles. He also stated that "by cortical stim-
ulation, the true antagonists were never thrown into
simultaneous activity." Similar observations were re-
ported by other investigators, and it was agreed that
to produce solitary contraction of a muscle by cortical
(surface) stimulation was very difficult. It should be
noted, however, that there were many limitations in
pursuing these experiments. The stimulation used at
that time was faradic current produced by induction
coils. With this instrument, frequency and duration of
the pulses were determined by the rate of vibration of
the contact breaker, whereas the intensity was varied
by changing the distance between two coils. Because
of the sparking at the make and break of the circuit,
however, accurate control of stimulus parameters was
impossible. To make the situation worse, the only
anesthetics available were chloroform and ether, with
which control of the depth of anesthesia was very
difficult. Altogether the results supported Jackson's
notion that movements rather than muscles are rep-
resented in the motor cortex, i.e., "the nervous system
knows nothing of muscles and thinks in terms of
movement" (158).
In 1947 Chang et al., aided by the rapid progress of

B
Toes Sulcus
Ankle,', I cen~.olos
Anus 8< Vagina" "
kne.e.--_

E!lelod /
Nose I \ ' Sulcus centrolis
Vocal \
co.ds Masbcation

FIG. 1. A: Ferrier's historic map of motor representation of monkey brain (46). 1, Opposite hindlimb
is advanced as in walking. 2, Flexion with outward rotation of thigh, rotation inward of leg, with
flexion of toes. 3, Tail. 4, Opposite arm is adducted, extended, and retracted; hand pronated. 5,
Extension forward of opposite arm; a, b, c, d, movements of fingers and wrists. 6, Flexion and spination
of forearm. 7, Retraction and elevation of angle of mouth. 8, Elevation of ala of nose and upper lip. 9
and 10, Opening of mouth with protrusion, 9, and retraction, 10, of tongue. 11, Retraction of angle of
mouth. 12, Eyes open widely, pupils dilate, and head and eyes turn to opposite side. 13 and 13', Eyes
move to opposite side. 14, Pricking of opposite ear, head and eyes turn to opposite side, pupils dilate
widely. B: motor representation in brain of chimpanzee. Left hemisphere viewed from side and above
to obtain best configuration of sulcus centralis area. Motor area indicated by stippling. Shaded
regions, marked EYES, indicate portions of cortex that yield conjugate movements of eyeballs under
faradization. S.F., superior frontal sulcus; S.Pr., superior precentral sulcus; I.Pr., inferior precentral
sulcus. [A from Ferrier (46); B from Sherrington (137).]
 CHAPTER 15: THE PYRAMIDAL TRACT 705

electrical techniques, made an important observation s s

(33). They were able to control the stimulus param-
eters, i.e., frequency, intensity, and pulse duration,
independently and were able to elicit an isolated re-
sponse of a single muscle without the simultaneous
contraction of any of the other muscles under obser-
vation (Fig. 2). The results clearly demonstrated top-
ographical representation of muscles within the motor

r
cortex, although the mode of representation was dif-
ficult to assess. They concluded that the Betz cells (by
which they meant pyramidal tract cells) for a partic-
ular muscle were distributed over an area of the cortex
with the highest cell concentration located at a partic-
ular focus within this area.
Another complication relating to the use of cortical
-+~DII
• H •
• 0
+ •

~t
surface stimulation is the difficulty of determining
which neuronal element is activated when electrical
current is passed from the surface. Patton and Amas-
sian (123), using monkeys, studied this problem by
recording corticofugal volleys elicited by bipolar cor-
tical stimulation. They recorded a stable, short-la- ~
tency, short-duration, positive deflection (D-wave),
which was followed by a series of irregular rhythmic
waves (I-waves) lasting for several milliseconds (Fig. FIG. 3. Pyramidal tract responses (R) to stimulation (8) of motor
cortex and white matter in monkey. Recording electrode in lateral
column of spinal cord at fIrst cervical segment. Downward deflection
indicates positivity at electrode in pyramidal tract. Time: 1 ms.
.... \ Direct (D) and indirect (I) waves present at left, whereas only D-
o ., wave at right. [From Patton and Amassian (123).]
'. • Belz cell for Il'IJscle I
o Belz cell for Il'IJsde 2
o 1
G Belz cell for muscle 3 3). They presented convincing evidence that the first
• Belz cell for muscle 4 wave was elicited by direct activation of pyramidal
tract neurons and the later waves were caused by their
indirect excitation. The results clearly indicated that
"bipolar" cortical surface stimulation excites pyrami-
dal tract neurons directly and also synaptically
through cortical intemeurons.
This combined direct and synaptic activation of
M.I pyramidal tract neurons would complicate the inter-
pretation of experiments using cortical surface stimu-
lation. These interpretative difficulties were reduced
"'.2 by the efforts of Phillips and his collaborators (67, 87).
Instead of using bipolar stimulation, Hem et al. (67)
used monopolar anodal stimulation and were able to
_ _ _ _ ---A- activate pyramidal tract neurons only directly. Using
"'.3 this technique of monopolar stimulation, Landgren et
al. (87) recorded monosynaptic excitatory postsyn-
".4 _--L aptic potentials (EPSPs) from cervical motoneurons
in the monkey. Instead of simply mapping the low-
Focus A Focua B threshold areas on the cortex, they measured the size
limillli medium strona Iimillli medium strona
stim. stim. stim. stim. stim. stim. of EPSPs elicited in a given motoneuron by an elec-
FIG. 2. Diagrammatic representation of hypothetical distribu-
trode moved over the cortical surface to determine the
tion of pyramidal tract cells for individual muscles. Cell group for extent of current spread within the cortex. Then they
each muscle has focal distribution and overlapping fringe. Each calculated the focal areas. They concluded that in
symbol represents a pyramidal tract cell. Large concentric circles about one-half of the instances studied, colonies of
are spheres of excitation. Expected contraction of muscles to cortical pyramidal tract neurons that projected monosynapti-
stimulation at different strength shown by myograms in lower
portion, in which magnitude of contraction is determined by number cally to single spinal motoneurons were confined
of pyramidal tract cells involved in sphere of excitation. [From within narrow foci having a cross-sectional diameter
Chang et al. (33).] of the order of 1.0 mm (Fig. 4). In the remainder of
706 HANDBOOK OF PHYSIOLOGY - THE NERVOUS SYSTEM II

those of Landgren et al, (87), who reported that about

one-half of cervical motoneurons studied received
monosynaptic inputs from a restricted cortical area.
The results also are not concordant with those of
Chang et al, (33), who reported that isolated contrac-
tion of single muscles could be elicited by stimulation
of circumscribed cortical areas. These apparently con-
tradictory results have been to some extent resolved
by Asanuma et al, (13), who demonstrated that the
surface threshold currents (0.3 rnA) for activating a
given pyramidal tract cell did not change within an
area of 2.0 mm in diameter, With 004 rnA, individual

..
pyramidal tract cells could be activated from areas as
,

...
, wide as 4 mm in diameter. This was partly due to the
, activation of pyramidal axon collaterals that were
found to spread nearly LO mm from the cell body and
, , '0' to have an excitability as high as the cell or initial
10 5 0 5 10 segment of the axon. These experiments were carried
out using cats. Because it is known that minimum
mm
thresholds for activating pyramidal tract cells from
FIG. 4. Amplitude change of monosynaptic excitatory postsyn- the surface of the cortex are approximately equal in
aptic potentials (EPSPs) recorded in radial motoneuron of baboon. cats (67) and monkeys (66), the projection areas re-
Amplitude plotted against distance from best point. Large curves, ported by Jankowska et al, (75) could have been
stimulus 1.3 rnA; small curves, stimulus 0.75 rnA; membrane poten-
tial -66 mY. Dotted line, points along line at right angles to smaller than they estimated. Asanuma et al, (13) con-
Rolandic fissure; unbroken line, points parallel to Rolandic fissure. cluded that surface stimulation could not resolve the
Upper right: points of stimulation around Rolandic fissure. Large question as to whether a single muscle is represented
circle, best point. Arcs show farthest limits of cell populations in the motor cortex,
excited by stimuli applied at points of zero synaptic action on test
motoneuron. [From Landgren et al. (87).]
Apart from this question of single muscle represen-
tation, investigators have generally agreed that motor
function is represented topographically within the cor-
the cases, however, these colonies were widespread in tex, This organization has been studied most exten-
the motor cortex, Jankowska et aL (75) restudied the sively by Woolsey and his collaborators (163), who
same problem in lumbar motoneurons of the monkey performed comparative studies on the localization of
using computer averaging technique, They stimulated cortical sensory and motor functions. A typical exam-
the surface of the cortex with single anodal pulses of ple of their results is shown in Figure 6, They also
near-threshold strength for pyramidal tract cells (004- studied the origin of the pyramidal tract, As already
0,5 rnA), assuming that the spread of current was stated, the Marchi method reveals only the degener-
limited to within a distance of LO mm from the elec- ating myelinated fibers, In addition, because only
trode, The area of origin of pyramidal tract cells about 10% of the pyramidal fibers are large enough
projecting to a given motoneuron was defined as that (> 51l.m) to show up with this technique (89), accurate
area from which were evoked EPSPs of at least 30% location of the origin of the smaller fibers was uncer-
the amplitude of the largest monosynaptic EPSPs, tain. Woolsey and Chang (162) developed an elegant
They reported that cortical areas projecting to a mo- method of stimulating the medullary pyramid and
toneuron were remarkably large, most often between then examined the distribution of antidromically
3 mm 2 and 7 mm 2 (Fig, 5). They also reported that evoked potentials on the surface of the cortex. As
areas of location of pyramidal tract cells projecting to shown in Figure 7, these potentials are not restricted
various motoneurons innervating one muscle were to the precentral (primate) or pericruciate (carnivore)
usually not identical. These areas often overlapped gyrus, the sites of the classic motor cortex, but spread
only partially or did not overlap at all. A problem in over the sensory as well as premotor areas. From these
the interpretation of their results (75) is that if each findings, as well as from the known evidence that
area actually occupies 3-7 mm 2 (average of 5 mm 2 ) stimulation of the sensory cortex with stronger cur-
and there is no overlap, then the total area necessary rents can produce movements and that peripheral
for innervating even one motoneuron pool [260 a- nerve stimulation evoked potential changes in the
motoneurons in medial gastrocnemius nucleus (31)] motor cortex, Woolsey (161) proposed the terminology
becomes so large that it cannot be fitted into the sensory-motor and motor-sensory to describe the clas-
motor cortex. Therefore some assumptions are neces- sic sensory and motor cortices, respectively. These
sary, such as the possibility that only a small fraction terms are still used by many investigators and need to
of motoneurons receives cortical innervation. Another be distinguished from the also-common term sensori-
difficulty is that the results apparently differ from motor, which refers to the sensory plus motor cortices.
 CHAPTER 15: THE PYRAMIDAL TRACT 707

L L
A 0·4 rnA ' _ 6 B 0·5 rnA ----- 6

FIG. 5. Area of origin of pyramidal tract

cells projecting to a lateral gastrocnemius
motoneuron in monkey. A, B: averaged rec-
-I'-- 3 ords of postsynaptic potentials evoked from
indicated electrode positions by 0.4 and 0.5
rnA, respectively. C, D, E: comparison of
total projection areas and areas from which
2 largest excitatory postsynaptic potentials
1·5· (EPSPs) were evoked at O.4-mA strength
for illustrated lateral gastrocnemius moto-
L L L neuron and for motoneurons to synergistic
6 muscles (MG, medial gastrocnemius; PI,
C 6 D 6 E plantaris) and to antagonistic muscle (DP,
5 5 5 deep peroneal). [From Jankowska et a1.
4 (75).]
4 4
3 3 3
2 2 2
1 1 1
0 0
R 6 5 4 321 0 R6 5 4 3 2 1 0 R 6 5 4 3 2 1 0

Studies by Cortical Depth Stimulation of interpretation of the results of surface stimulation

experiments mentioned earlier. To activate pyramidal
Although Betz cells are known as the origin of fibers tract neurons, the current has to travel at least 1.2 mm
in the pyramidal tract, these cells contribute only 3% from the surface and when the neuron is located deep
or 4% of the total pyramidal fibers (89). They have in the sulcus, the distance is even greater. This large
been identified as a part of the origin of the tract by distance created ambiguity in the attempts to localize
the occurrence of retrograde cellular changes after motor function because of uncertainties about the
pyramidal section. The difficulty intrinsic to this effective current spread. The difficulty has been over-
method is that not all affected cells present changes come by directly stimulating the depth of the cortex
that are definite enough to permit recognition. This is through metal microelectrodes. Stoney et al. (141)
particularly true with small pyramidal tract cells. Be- could excite pyramidal tract cells directly and/or syn-
cause of these limitations, the analysis of the laminar aptically through a microelectrode with currents of
distribution of pyramidal tract cells had been limited only microamperes, less than one-hundredth of the
to physiological experiments in which the depth dis- current necessary to activate the same cells from the
tribution of antidromic unitary activities was exam- surface. Because the current necessary for activating
ined. In the early stages of microelectrode experi- pyramidal tract cells was so weak, it could be delivered
ments, there were reports that pyramidal tract cells through fine microelectrodes that were also able to
were located in both layer III and layer V. The latest record unit spikes. By using a pair of microelectrodes,
and most extensive analysis made using microelec- one for microstimulation of and the other for extra-
trode techniques (71), however, suggests that at least cellular recording from a given pyramidal tract cell,
the majority of pyramidal tract cells, both large and Stoney et al. were able to examine the spread of
small, are located in layer V in the monkey. Using stimulating current within the cortex. Negative cur-
retrograde transport of horseradish peroxidase after rent was found to be more effective for depth stimu-
injections into the spinal cord, Coulter et al. (36) were lation. When the stimulating current was restricted to
able to stain large- and medium-sized pyramidal tract 10 /LA or less (0.2-ms duration), direct excitation was
cells in cats and monkeys and reported that they were limited to those cells located within a distance of less
all located in layer V. This study strongly supported than 0.1 mm, and synaptic activation was limited to
the conclusion that all corticospinal tract fibers origi- within a radius of less than 0.5 mm.
nate from pyramidal-shaped cells in layer V. They are Utilizing the intracortical microstimulation tech-
located at a depth of 1.2-2.0 mm from the surface in nique, Asanuma and his collaborators examined the
the monkey and slightly shallower in the cat because localization of motor function in the cat (12) and the
of its thinner motor cortex. monkey (10). Figure 8 shows an example of the results
These findings may explain some of the difficulties obtained using anesthetized cats, where the' effects of
708
 CHAPTER 15: THE PYRAMIDAL TRACT 709

A 8
FIG. 7. Distribution of potentials produced by antidromic activation of pyramidal tract neurons by
stimulation of medullary pyramid in cat, A, and monkey, B. Potentials are not restricted to motor
cortex. [From Woolsey and Chang (162).]

microstimulation were monitored by its facilitation or
inhibition of spinal monosynaptic reflexes. At the
depths from 0.5 rom to 1.1 mm, 20-ItA stimulation
facilitated extensor digitorum longus (wrist dorsi-
flexor) reflexes with the lowest threshold at 1.0 rom.
At this depth, stimulation with 20 itA also facilitated
extensor carpi ulnaris and extensor carpi radialis re-
flexes. Weak stimulation (less than 10 itA), however,
produced the effect only on extensor digitorum longus
reflexes. This is the major difference between the
effects of microstimulation and surface stimulation.
Usually threshold microstimulation produces the ef-
fect only in one motoneuron pool, whereas surface
stimulation, even with threshold intensity, produces
effects in more than one motoneuron pool. It was also
shown that the effect of microstimulation was abol-
ished by pyramidal section (12). Altogether, the results
suggested that there are aggregates of pyramidal tract
cells in small areas of the cortex which send their
axons to particular motoneuron pools, and also sug-
gested that these cells are intermixed with others
projecting to different motoneuron pools. In the ex-
ample shown in Figure 8, the area for the extensor
digitorum longus was limited to a small focus, but the
area for the extensor carpi uloaris was wider and had
two foci.
Asanuma and Sakata (12) were also able to delineate
the extent of low-threshold cortical areas that facili-
tated a particular monosynaptic reflex in the cat. The
lowest threshold sites were confined within a sector
that extended along the direction of the radial fibers
in the gray substance. The diameter of the sectors
ranged from 0.5 mm to a few millimeters, the average
being about 1.0 mm, and the fringes overlapped with
those of neighboring sectors. Figure 9 shows an ex-
ample of such a sector, which was termed a "cortical
efferent zone." The lowest threshold points in adjacent
penetrations were located along a line parallel to the
radial fibers, and the threshold increased rapidly as
the electrode was moved. At the fringes thresholds
suddenly rose to greater than 20 itA. A similar arrange-
ment was found in the monkey cortex. In these exper-
iments (10) the effect of cortical stimulation was mon-
itored by electromyographic recordings as well as by
observing movement of fingers. In adjacent penetra-
tions the effective sites for eliciting extension and
adduction of the thumb were located in an area par-
allel to the radial fibers in the gray matter (Fig. lOA).
When the stimulus intensity was doubled (Fig. lOB),
the distribution of the effective sites was more com-
plicated. The area for thumb flexion expanded into an
irregular shape, and two areas for thumb abduction
were found. The authors suggested that the abduction
of the thumb produced by stimulation of the second
area was possibly due to the sum of the contractions
caused by simultaneous activation of neighboring ex-
tension and flexion zones.
In their experiments Asanuma and collaborators
(10, 12) used only weak intracortical microstimulation
of 10 ~ or less and identified only the lowest threshold
efferent zones. On the other hand, Andersen et al. (7),
using stronger intracortical stimuli (80 itA or less) in
the lightly anesthetized monkey, were able to activate
the same muscle units from different cortical foci,

FIG. 6. Composite figurine charts of precentral and supplementary motor areas of monkey brain
derived from several experiments in which left cortex was mapped by systemic punctuate electrical
stimulation. C, central sulcus; area between C and C' folds down to depth of sulcus. d, Medial edge of
hemisphere; area between e and e' is supplementary motor area located on medial surface of
hemisphere. Except for responses from points in ipsilateral motor face area (at extreme left), muscle
responses are on right side of body. Strongest and earliest movements indicated in solid, intermediate
in cross-hatching, and weakest in stippling. Symbols with crosses on ankles indicate eversion of foot;
symbols with open centers on hip and ankle signify adduction and inversion; curved lines with arrows
designate rotation. e, Sulcus cinguli; i, inferior precentral sulcus. [From Woolsey et al. (163).]
710 HANDBOOK OF PHYSIOLOGY - THE NERVOUS SYSTEM II

..
I'A
o EDL

,
/
xECU /
/

~ECR
z 6 CEOC
o 7
~ 8
t: 10

!§ 12

~
IS
20

N~i~t\!

0.5 1.0 1.5 2.0 mm

I I I I I

DEPTH
FIG. 8. Threshold changes for facilitation or inhibition of 4 spinal monosynaptie reflexes during
insertion of stimulating microelectrode into cortex in cat (top right inset). Ordinates, threshold
currents (p.a) for just-observable facilitation (upper graph) and inhibition (lower graph). Note that
graphs symmetrically reach maximum current of 20 /La bordering hatched area, which indicates no
effects with stimulation of 20 /La. EDL, extensor digitorum longus; ECU, extensor carpi ulnaris; ECR,
extensor carpi radialis; EDC, extensor digitorum communis. [From Asanuma and Sakata (12).]

although with different thresholds. Using squirrel
monkeys, Strick and Preston (147) examined the dis-
tribution of efferent zones with weaker current of 10
/-LA or less. They reported that finger areas and wrist
areas were mutually intercalated with small bands of
0.25-mm width. The same movement was represented
twice in the small area of the motor cortex. The
difference in thresholds reported by Andersen et aI.
(7) may indicate that the density of neurons projecting
to a particular motoneuron pool varies among the
different foci. Kwan et aI. (86), using unanesthetized
awake monkeys, mapped motor representation with
the microstimulation technique. They reported that
finger zones were tightly clustered in a central area
surrounded by loci evoking movement about the wrist.
They concluded that there is a nested-ring organiza-
tion of the forelimb zones in the motor cortex such
that a cortical zone controlling movement of a distal
joint is partly encircled by the zone controlling a more
proximal joint. The microstimulation method has thus
enabled the delineation of progressively finer details
of organization of efferent zones in the motor cortex.
To evoke motor effects from the cortex necessitates
repetitive stimulation. Therefore consideration must
be given to the extent of effective spread of such
repetitive stimulation and to the means by which it
activates corticofugaI neurons. From the time of some
of the earliest studies utilizing intracortical micro-
stimulation, it has been known that even weak stimuli
may excite pyramidal tract neurons not only directly
but also synaptically (141). For the purpose of exam-
ining the relative contributions of these modes of
activation, Jankowska et al. (74) recorded descending
volleys from the lateral funiculus of the spinal cord
following cortical stimulation. As shown in Figure 11,
the direct response did not change much during repet-
itive stimulation, but the indirect (synaptic) responses
to the second and third stimulus presentations were
much larger. Similar results were reported by Asan-
uma et al. (13), whose studies showed that micro-
stimulation delivered to the pyramidal tract cell layer
produced both direct and indirect descending volleys,
but only indirect waves when delivered to the super-
ficiallayers. During repetitive stimulation, the synap-
tic responses were grouped in one volley after each
stimulus. Judging from the latencies, Jankowska et al.
(74) concluded that "practically all of the earliest
indirect and a great part of the later responses" were
 CHAPTER 15: THE PYRAMIDAL TRACT 711

A B
6 4 3
- .........
~ Post·cruci ate Pre·cruclate

76 2
• ••••
•
431
•5

mm 5 mm
FIG. 9. Distribution of low-threshold points for facilitation of monosynaptic reflexes in medianus
pronator nerve (pronator of wrist). A: tracks that passed low-threshold points of less than 20 lUi. Each
track number corresponds to surface position shown in B. Numbers along penetrations show threshold
currents. [From Asanuma and Sakata (12).]

induced monosynaptically. If an indirect (and mainly
monosynaptic) activation of pyramidal tract cells is
the predominant effect of intracortical microstimula-
tion, it becomes important to consider the extent of
the monosynaptic spread from the site of stimulation.
It is known that neurons in the cerebral cortex are
connected predominantly in the radial direction (99),
with the spread of fibers in the horizontal direction
being limited to a short distance (35, 99, 149) except
for layer I. Figure 12 shows cells and their intercon-
nections in the neocortex as drawn by Szentagothai
(149). The connections are mostly in the radial direc-
tion, and the only horizontal spread is in the deep
layer by basket cells, which probably act as inhibitory
neurons. As the motor effects of microstimulation
appear from layer II or deeper, the horizontal spread
of impulses in these layers is of interest. This has been
studied by Asanuma and Rosen (11) by stimulating
the cat cortex with a microelectrode at various depths
and recording postsynaptic potentials from nearby
neurons through another electrode. They found that
monosynaptic spread from the superficial layers (II,
III) was limited to neurons located within a horizontal
distance of 0.5 mm from the stimulation site. Stimu-
lation of the deep layers (V and VI) produced mono-
synaptic postsynaptic potentials (PSPs) in neurons of
the same layer as well as in the superficial layers, and
the horizontal spread was wider. This wider spread
was mostly inhibitory, however. Microstimulationalso
produced polysynaptic PSPs in neurons of wider areas,
but the effects beyond the monosynaptic range were
predominantly inhibitory. Hess et al. (68) microion-
tophoretically ejected small amounts of glutamate into
the visual cortex in the cat to excite a small group of
neurons and reported that the effects upon neighbor-
ing cells were predominantly inhibitory. The possibil-
ity that association fibers produce corollary activation
of neurons in distant regions of the motor cortex seems
small, because a microlesion of the motor cortex pro-
duces degenerating fibers only in the vicinity of the
lesion (55). Taken together, the results suggest that a
train of microstimulation pulses activates corticofugal
neurons mostly transsynaptically, but also suggest
that these activated neurons are located within a
horizontal radius of about 0.5 mm from the stimulating
electrode.
Recent development in anatomic techniques has
made it possible to examine the structural basis for
the localization of motor function. Using the Nauta
method, Kuypers and Brinkman (85) showed that a
712 HANDBOOK OF PHYSIOLOGY -
FIG. 10. Distribution of effective spots for pro-
ducing thumb movements within depth of motor
cortex. Effects examined at lOO-J.lm steps in each
penetration. A: Examined with stimulating current
of 5 J.la. B: examined with 10 J.la; 0, thumb flexion;
0, thumb extention; ., thumb adduction; ., thumb
abduction; -, spots of no effect. [From Asanuma
and Rosen (10).]
lesion in either the forelimb or hindlimb area of the
precentral cortex produced degeneration of fibers at
all levels of the spinal cord but that the common
regions of distribution were restricted to parts of the
spinal gray matter outside the motor nuclei. Those
fibers terminating within the cervical or lumbar motor
nuclei originated only from the respective forelimb or
hindlimb area of the precentral cortex. More recently,
Groos et al. (60) injected horseradish peroxidase into
different spinal segments in the cat and observed that
5-10 labeled neurons formed clusters having diameters
of 0.3-0.5 mm, which they interpreted as a sign of
functional subdivision within the motor cortex. Neu-
rons projecting to the spinal enlargements were most
abundant in area 4, the primary motor cortex; but
substantial populations of neurons were located also
in areas 1, 2, 3, and 6, and labeled neurons included
large and small pyramidal cells of layer V.
Microstructure of Corticospinal Projection
Data presented in the preceding section lead to the
conclusion that there is a fine localization of cortical
motor function at the level of individual muscles,
especially for the distal limb muscles. It cannot be
concluded, however, that all projection neurons within
a given cortical efferent zone terminate only in a
particular motoneuron pool. On the contrary, the ob-
servation that stronger microstimulation even at the
center of a cortical efferent zone produces contraction
of more than one muscle suggests that neurons pro-
jecting to different motoneuron pools are intermixed
in a given efferent zone.
In addition to this issue of the projections of neigh-
boring corticospinal neurons, there is the remaining
fundamental question of whether or not individual
corticospinal neurons synapse only with motoneurons
innervating one muscle (41). Several attempts have
been made to answer this question. Scheibel and
Scheibel (134) stained terminal branches of presumed
corticospinal fibers of the cat using the Golgi-Cox
method. They observed that both collateral and ter-
THE NERVOUS SYSTEM II
M-Cx M-Cx
4 5 10 15
4 5 10 15
\
\
\
\' \ 1111 11111 1111111111
b
minal branches of individual fibers left the body of the
corticospinal tract and entered the spinal gray matter
at right angles over a distance of one to three segments
and terminated on interneurons within the interme-
diate zone (Fig. 13). These interneurons, in turn, pro-
jected from one to four segments rostral and caudal,
and frequently in both directions. Futami et al. (54)
observed similar patterns of branching following injec-
tions of horseradish peroxidase into single pyramidal
tract fibers in the spinal cord in the cat. These findings
could be interpreted to indicate that some pyramidal
tract neurons exert influences on spinal motoneurons
located in a small area within one segment, whereas
others can exert the effects over as many as 6-8
segments through interneurons. As a given motor nu-
cleus that innervates a muscle extends from one to
three segments along the spinal cord (31, 132), the
results suggest that some pyramidal tract neurons can
influence more than one motor nucleus. However,
these studies were made with the cat, in which the
pyramidal tract is known not to make direct synaptic
connections with motoneurons (98), and there is a
possibility that some interneurons on which the py-
ramidal tract axons terminate do not have connections
with motoneurons. Subsequently Shinoda et al. (139)
performed electroanatomic experiments in monkeys
in which pyramidal tract cells were activated antid-
romicallY from branches located within spinal motor
nuclei. They found that about one-third of the pyra-
midal tract neurons sending axons to cervical motor
nuclei also sent other axon branches to the lower levels
of the spinal cord. Those pyramidal tract neurons
terminating only within the cervical cord branched
extensively, and nearly one-half of the neurons distrib-
uted axons to more than one segment. Some sent
branches as widely as three segments of the cervical
ventral horn. It was also found, however, that pyra-
midal tract neurons activated from the various motor
nuclei were not alike, i.e., those activated from within
motor nuclei innervating distal forelimb muscles
branched significantly less than those activated from
nuclei innervating proximal muscles.

A F
~]
..:---'\.~
" ::
B
"4 1 '*-.'.......
C H
~ -"'---:" ~';
..--'; .r \ r:""'
I '
D . , \j
~ .~
... \1
• 1
-'r-'.~ ,/.j /1
J . '"
• r •
! ': V! / records at right. Amplitude of stimuli shown at
:i ' .: i:
E~
-- ................... -- \;
-r-,--r
J'TT"'TTTTTT
1+S msec
(A-D)
Fetz et al. (48, 49) studied this problem using a
different approach. Their rationale was that because
pyramidal tract neurons have direct connections with
motoneurons in primates, the activity of a given py-
ramidal tract neuron would change the excitability of
the motoneurons upon which it terminated, so that
following the pyramidal tract neuron discharge, the
firing probability of these motoneurons would be in-
creased. This change of motoneuronal firing frequency
would be detectable by averaging unitary electromy-
ograms. With this assumption, they implanted elec-
trodes into various muscles of awake monkeys and
could observe transient increases of electromyographic
activity in more than one muscle following discharges
of individual pyramidal tract cells in the motor cortex.
The results suggested that at least some pyramidal
tract neurons send terminal branches to more than
one group of motoneurons innervating different mus-
cles. The results have to be interpreted with some
caution, however. It is known that a group of cortical
neurons located within a limited area receive similar
inputs in the sensory (70, 113) as well as in the motor
(27, 28, 133) cortices in both cats and monkeys. It is
possible that some pyramidal tract cells receive the
same inputs from the same source and produce syn-
chronous discharges, even if only occasionally. Be-
cause the averaging of the electromyograms was made
for several thousands of pyramidal tract cell dis-
charges, a possibility exists that the transient facilita-
tion in different muscles was produced by different
pyramidal tract neurons. Although the authors (49)
were aware of the problem, it is difficult to exclude
this possibility completely. Thus, all the results until
now are inconclusive as to whether a single pyramidal
tract neuron terminates upon different groups of mo-
CHAPTER 15: THE PYRAMIDAL TRACT 713
..i'\..
FIG. 11. Descending volleys evoked by repeti-
tive intracortical stimulation in monkey. A, F: an-
" • tidromic potential from pyramidal tract cell. B-D,
G-J: descending volleys evoked by increasing
( strength of stimulation at same electrode position
as in A and F, recorded from lateral funiculus at
i ~
L,-L2• J: intracortical stimulation with same
' strength as for D and I, but 300 Iill1 deeper. Super-
imposed traces at left and corresponding averaged
...; . i
right, and their timing on lower traces in D and J.
Arrows indicate direct responses to cortical stim-
~-..j
] ulation, negativity downward. [From Jankowska et
~V al. (74).]
10 JlA
r Iii i I
1+S msec
(F-J)
toneurons innervating different muscles, but they sug-
gest that at least some pyramidal tract neurons do so.
A natural question then arises regarding how these
pyramidal tract neurons innervating various groups of
motoneurons are organized within the motor cortex to
produce movements. To investigate this question, As-
anuma et al. (20), using anesthetized monkeys, re-
corded antidromic spikes simultaneously from a group
of pyramidal tract cells through an electrode placed in
a fixed position in the motor cortex and traced the
branches of these pyramidal tract neurons in the spinal
cord. They made a grid of microelectrode insertions
into the spinal cord and delivered weak stimulating
currents to activate these pyramidal tract cells anti-
dromically. By adjusting the dimensions of the grid
and the intensity of stimuli, they could activate all
branches within given areas. Because the stimulating
electrode could also be used to record antidromic field
potentials from spinal motor nuclei, they could relate
the locations of pyramidal tract branches and of motor
nuclei. An example of the results is shown in Figure
14. Four pyramidal tract cells were simultaneously
recorded through the same electrode, indicating that
these cells were located close together. Three of them
sent branches to the spinal motor nuclei as well as
outside the nuclei, and one, marked by the parallelo-
gram, sent branches outside the nuclei only. As shown
in Figure 14A and summarized in Figure 14B, all three
neurons sent terminal branches to nucleus extensor
digitorum brevis and all three passed through nucleus
flexor digitorum longus. If the sites of synaptic con-
tacts between pyramidal tract axons and motoneurons
is limited only to soma or proximal dendrites, the
results could indicate that a given pyramidal tract
neuron synapses with motoneurons innervating differ-
714 HANDBOOK OF PHYSIOLOGY - THE NERVOUS SYSTEM II

Ilt
Assoc. call.
aff.
,,

FIG. 12. Interconnections of some cell types in cerebral cortex. Two pyramidal cells shown in
laminae 3 and 5. Specific afferent fiber (spec. aff.) shown to excite stellate cell (SI), the axon of which
establishes cartridge-type synapses on apical dendrites. Specific afferent fiber also excites stellate
interneurons (S3) that give inhibition to pyramidal cells in adjacent cortical columns, indicated by
shadings. Sp, stellate pyramidal cells; S2, short axon inhibitory cells in lamina 2; S5, S6, interneurons
with ascending and descending axons. [From Szentligothai (149).]

ent muscles. The exact site of synaptic contact, how-

ever, is unknown, and if some pyramidal tract fibers m -------------- -----.- ((2)j~
synapse on distal dendrites, the location of apparent p ~---.
terminal branches does not reflect a connection be-
tween the pyramidal tract fibers and identified motor
nuclei. This caution is necessary because motoneu-
rons, especially those with large cell bodies, send den-
dritic branches several millimeters from the soma,
spreading even into the intermediate zone of the spinal
cord (134). With these limitations in mind, Asanuma
et al. (20) examined the distribution of spinal branches
of four groups of pyramidal neurons and found that in
all cases there was at least one motor nucleus in which
the majority of the neurons sent branches that either
terminated there or passed through. Because of tech- c
nical limitations they could not determine if those
fibers that passed through a common nucleus made
synaptic contacts with nearby neurons by short
FIG. 13. Terminal branches of pyramidal tract axons in lumbar
branches, but the possibility does exist. A similar cord of cat. Horizontal section cut slightly obliquely (inset diagram)
organization has been reported in the pyramidal tract showing relations of lateral corticospinal terminals (f') to propri-
system of the cat in which a group of pyramidal tract oneurons. Terminating corticospinal elements, c, project synapti-
neurons located close together tended to be activated cally upon lateral dendrites and somata of propriospinal neurons d
and e. At arrow, terminals from two different corticospinal fibers
antidromically by stimulation through the same elec- converge on same dendrite. Propriospinal neurons d and e project
trode in the spinal cord (138). The results altogether axons toward midline, m, and/or lateral propriospinal bundles, p, to
suggest that although pyramidal tract axons from a form secondary terminals, f2. [From Scheibel and Scheibel (134).]
 CHAPTER 15: THE PYRAMIDAL TRACT 715

A B

1'r
OUTSIDE
NUCLEI MOTOR NUCLEI

l:r 1~1
TA-

l§l FOL PER LG MG SOL TlB

o L-6 : : : I : :
I I I I I I
TA-EDL I I I I I I
: : I : : I
I , I I I
I I I I I
I I I I I
I I I I I I I
I 1 I I " I I I

111 Id 1:111 fl n
EDB -
PER
TA-EDL
L-7 I I
I
I
I
I
I
I I
I,
I I
I
I
I
I
I
1 I
I
11
,
I
0

:: : 1 : I I I I I : ' :
I I ,I' I I I I 1 I I I
I I I I I It' I I I I
I I I 1 I I I I I I I, I I I I

uuu u11 n11

I I I I I I I I , I 1 I I I 1 1
o
PER
SOL
lil I I : :
11 ':
I I I I I
o S-l : I I I I I I

TIB

U1111 1-1 11
SOL

1°1 [lOmm
FIG. 14. Distribution of terminal branches of 4 pyramidal tract neurons in spinal cord. These 4
neurons recorded simultaneously through same cortical electrode. A: likely course of axonal branches
summarized in 4 representative transverse planes. Each neuron represented by different line and
symbol. B: areas of passage (open symbols) and termination (filled symbols) of axon collaterals in
ventral hom in relation to motor nuclei identified by antidromically evoked potentials. Continuous
bars, explored parts of spinal cord; dashed bars, unexplored areas; OTHER, those sites that
histological examination indicated as ventral horn, but antidromic stimulation of isolated motor
nerves did not identify nuclei. FDL, flexor digitorum longus; EDB, extensor digitorum brevis; EDL,
extensor digitorum longus; PER, peroneus; LG, lateral gastrocnemius; MG, medial gastrocnemius;
SOL, soleus; TIB, tibialis; 1.., sixth lumbar segment; L7 , seventh lumbar segment; S" first sacral
segment. [From Asanuma et al. (20).]

small area in the motor cortex project to a wide area
in the spinal cord, there is a focal area to which they
project most heavily. Figure 15 illustrates the above
conclusion in a simplified form.
Projection to y-Motoneurons
The cortical representation of y-motoneurons was
first studied by Mortimer and Akert (111) in anesthe-
tized cats and monkeys. They recorded unitary activ-
ities from lumbosacral ventral root filaments and dif-
ferentiated a- and y-motoneurons by their physiolog-
ical properties. They reported that the cortical area,
which activated y-motoneurons, was comparable to
the one for a-motoneurons in both species. Because
they did not section the pyramidal tract, however, it
still remained in question whether the effect was me-
diated by this tract. Fidone and Preston (50), using
pyramidal cats, and Grigg and Preston (59), using
pyramidal monkeys, examined cortical effects on y-
motoneurons. They dissected hindlimb nerves and
recorded unitary activities of both a- and y-fibers that
innervated the same muscle. They reported parallel
predominances of facilitation or inhibition on a- and
y-motoneurons of the same muscle. They also showed
(59) that there were monosynaptic connections made
by fibers of the pyramidal tract upon y-motoneurons
in primates. Clough et al. (34) stimulated the motor
cortex in the baboon and recorded intracellularly from
y-motoneurons that innervated distal forelimb mus-
cles. Of 19 y-motoneurons that they recorded, 6
showed EPSPs at monosynaptic latencies and 4
showed short-latency inhibitory postsynaptic poten-
716 HANDBOOK OF PHYSIOLOGY THE NERVOUS SYSTEM II

the sensory cortex end dorsomedially in the cord, in

laminae IV, V, and VI of Rexed (131). Neurons in
these laminae transfer afferent impulses from the pe-
riphery to local spinal segments and to higher levels
of the central nervous system. The fibers from the
motor cortex end in laminae V, VI, and VII in the cat
(119) and end further ventrally to lamina IX in the
monkey (84), where motoneurons are located. These
branching patterns suggest that the pyramidal tract
functions not only in transferring corticofugal impulses
directly to motoneurons, but also functions in modu-
lating reflex activities of the spinal cord. Furthermore,
those pyramidal tract fibers arising from the sensory
cortex may influence the transmission of afferent im-
pulses to higher centers, including the motor cortex.
This problem was studied most intensively by Lund-
FIG. 15. Simplified diagram showing mode of pyramidal projec-
berg and collaborators (102,103). They produced con-
tion from motor cortex to spinal motor nuclei (MN). Group of vincing evidence that the pyramidal tract and group
pyramidal tract neurons located in small area of cortex project Ia muscle afferents converge on the group Ia inhibitory
primarily to given motor nucleus, but some send axons to another pathway in cats (103). They used the conventional
motor nucleus and some send branches to more than one motor
nucleus.
method of conditioning monosynaptic reflexes by var-
ious stimuli. As shown in Figure 16, the inhibitory
tials (IPSPs), probably elicited by disynaptic connec- effect produced by deep peroneal nerve stimulation is
tions. Although they did not use pyramidal baboons, greatly enhanced by cortical stimulation. Because the
the monosynaptic EPSPs indicated that the transmis- cortical effect disappeared after pyramidal section,
sion was via the pyramidal tract. Thus the results they attributed the effect to the pyramidal tract. In
demonstrate the existence of y-representation in the the succeeding study (102), in which recordings were
motor cortex and show that at least some corticofusi- made intracellularly from spinal interneurons, they
motor connections are made through the pyramidal were able to demonstrate the convergence of inputs
tract. The overlap of alpha and gamma representa- from the motor cortex with those from skin and muscle
tions suggests that there is an a-y-linkage at the cor- afferents. Although they did not use pyramidal cats in
tical level. this experiment, they concluded that the effect was
The activity of y-motoneurons may be inferred by mediated by the pyramidal tract based on the short
monitoring discharges of spindle afferents. Koeze et latencies of the PSPs, which did not allow time for a
al. (83) examined cortical effects on spindle afferents disynaptic connection from the cortex to the target
using prolonged repetitive stimulation in the baboon. interneurons. The control of the spinal cord from the
They found both excitatory and inhibitory effects, but higher centers, including the pyramidal tract, has been
because they did not use pyramidal animals, other reviewed by Lundberg (100, 101).
pathways may have been responsible for the effects. The effects of cortical stimulation on spinal reflexes
in pyramidal cats and baboons were studied exten-
Projections to Spinallnterneurons sively by Preston and collaborators (130). Using the
conditioning-testing method, they reported that the
Although there are direct connections between py- amount of facilitation or inhibition produced by cor-
ramidal tract fibers and motoneurons in primates (22), tical stimulation was different in different motoneuron
the majority of the fibers terminate on spinal inter- populations. The pyramidal effect was predominantly
neurons (25). Those terminating on motoneurons arise inhibitory for extensor motoneurons and predomi-
primarily from pyramidal tract cells in the limb area nantly facilitatory for flexor motoneurons in both cats
and terminate on motoneurons innervating limb mus- and monkeys. This pattern, however, was reversed in
cles (84,96). Recent evidence indicates that even those motoneurons of the baboon. Preston et al. argued that,
innervating motoneurons send other branches outside although both the cat and the baboon are considered
the motor nuclei (Fig. 14). In cats the direct connection to be quadrupeds, the baboon uses the forelimb in a
to motoneurons has not been demonstrated (98, 119). manner similar to that of the erect primates. Because
In his pioneering study, Lloyd (98) elegantly demon- of these considerations, they suggested that the motor
strated, using the pyramidal cat, that pyramidal vol- cortex inhibits the tonic activities of postural mecha-
leys reached motoneurons through interneurons lo- nisms to permit volitional movements to occur.
cated in the intermediate region of the spinal cord. Thus· results from various laboratories demon-
The distributions of pyramidal tract axons arising strated that the pyramidal tract not only excites par-
from the motor and the sensory cortices are different ticular motor nuclei, but also exerts influences on
in both the cat and the monkey, suggesting a difference postural mechanisms of the spinal cord through inter-
of function between the two groups: those arising from neurons. The manner in which these specific and

H~ortell+ OP+
test
10 msec
general effects interact during natural movements is,
at present, rather difficult to assess. One of the seem-
ing paradoxes is that, although the electrophysiologi-
cal method has demonstrated connections between
the pyramidal tract and various spinal neurons, a
lesion of the pyramidal tract leaves very little func-
tional deficiency. As is discussed in more detail in
section FUNCTION OF PYRAMIDAL TRACT, p. 727, within
the first 24 h after a properly placed lesion, monkeys
can stand, grip the cage, and take a few climbing steps
(92). The only permanent deficiency is the loss of
discrete usage of individual digits. These findings serve
to remind us that the pyramidal tract is not the only
pathway from the higher central nervous system con-
trolling the movements or modulating the postural
mechanisms of the spinal cord. To what extent the
pyramidal tract participates in the postural control in
normal animals during willed movement is still in
question.
Pyramidal Collaterals and
Branches Within Brain
The pyramidal cells in layer V, including Betz cells,
are known to send axon collaterals as far as layer II.
The horizontal spread of these axon collaterals, how-
CHAPTER 15: THE PYRAMIDAL TRACT 717
FIG. 16. Pyramidal effects on gastrocnemius-so-
leus, G-S, and deep peroneal, DP, monosynaptic
reflexes. Reflexes were recorded simultaneously at
two different sweep speeds. Upper traces, reflex
discharges in ventral root; lower traces, potentials
at dorsal root entry zone. A: unconditioned test
A , reflex. B: effect of conditioning G-S reflex with
maximal group Ia volley in DP. C, D: effect of train
of 6 stimuli to motor cortex on A and B. E-H:
repetition of same series after transection of py-
ramidal tract shown in inset. [From Lundberg and
-..-JL A Voorhoeve (l03).]
p •
5 maee
ever, is limited to a narrow range of less than 1.0 mm
(99). Physiological experiments (13) have also dem-
onstrated that some pyramidal tract cells can be acti-
vated antidromically only from a horizontal distance
of less than 1.0 mm. The excitability of these axon
collaterals is as high as the neuron somata or axon
hillocks, and any cortical stimulation excites cell bod-
ies and axon collaterals indiscriminately (13). A ques-
tion then arises as to the manner in which these axon
collaterals influence neighboring corticofugal neurons.
Do they excite the neighboring pyramidal tract cells
or do they inhibit them in a way similar to that in
which spinal motoneurons inhibit the neighboring mo-
toneurons? Phillips (125) studied the problem by stim-
ulating the pyramidal tract with a strength subthresh-
old for an intracellularly recorded pyramidal tract cell.
Unlike ventral root stimulation, pyramidal stimulation
produced early depolarization followed by hyperpolar-
ization in the target cell. Later, Takahashi et al. (150)
demonstrated that this early EPSP is produced by
axon collaterals of slow pyramidal tract cells, which
synapse directly on the fast pyramidal tract cells.
Using lightly anesthetized cats or nonanesthetized cats
immobilized by coagulation of the brain stem, Stefanis
and Jasper (140) examined the effect of repetitive
stimulation of the pedunculus upon pyramidal tract
718 HANDBOOK OF PHYSIOLOGY - THE NERVOUS SYSTEM II
neurons. They found that repetitive antidromic stim-
ulation greatly enhanced the recurrent inhibitory ef-
fect, which lasted several tens of milliseconds after
stimulation. These inhibitory effects were frequently
interrupted by facilitatory effects. They suggested that
the recurrent inhibition by pyramidal tract axon col-
laterals functions to increase the contrast between a
central group of most active cells and the surrounding
neurons. Using unanesthetized cats, Brooks and As-
anuma (26) examined the effect of pyramidal stimu-
lation on the receptive fields of cortical neurons. They
demonstrated that the size of receptive fields of py-
ramidal tract neurons were reduced to the center of
the fields during and after repetitive stimulation of the
medullary pyramid.
Besides the recurrent axon collaterals, pyramidal
tract axons send branches to various subcortical nu-
clei. Until recently it was difficult to determine
whether the projection fibers to subcortical nuclei
were branches of pyramidal tract neurons or inde-
pendent fibers. Advances in electrophysiological tech-
niques have made it possible to determine whether
some of these projections are made by branches of
pyramidal tract axons. Tsukahara et al. (155) stimu-
lated the red nucleus in cats and were able to anti-
dromically activate pyramidal tract cells identified by
prior pyramidal stimulation. They also demonstrated
that pyramidal stimulation could produce EPSPs and
IPSPs in red nucleus neurons. Humphrey and Corrie
made an extensive study on the branching of pyrami-
dal tract axons by activating pyramidal tract cells from
the red nucleus in the monkey (71). They found that
the pattern of branching was different between fast
and slow pyramidal tract cells. About 20% of fast
pyramidal tract cells that they examined sent branches
to the red nucleus, whereas only 8% of slow pyramidal
tract cells sent branches. Because slow pyramidal tract
cells are more numerous than fast pyramidal tract
cells, they estimated that only about 10% of total
pyramidal tract cells send branches to the red nucleus.
In another study (72) they stimulated the pyramidal
tract and subcortical white matter after ablation of
the motor cortex in the monkey and reported that
subcortical stimulation exerted much bigger facilita-
tory effects upon red nucleus neurons. As subcortical
stimulation activated pyramidal as well as nonpy-
ramidal inputs to the red nucleus, they concluded that
the pyramidal collateral route is of only minor signif-
icance in activating red nucleus neurons. Endo et al.
(40) reported that some identified pyramidal tract cells
could also be antidromically activated from the corpus
striatum, ventrolateral or ventral posterolateral nu-
cleus of the thalamus, the red nucleus, the reticular
formation, or the pontine nucleus. Some pyramidal
tract cells could be activated from more than one of
these nuclei. In addition to the subcortical motor
nuclei, pyramidal tract branches reach sensory relay
nuclei. Jabbur and Towe (73) stimulated the sensori-
motor cortex in pyramidal cats and could excite or
inhibit neurons in the dorsal column nuclei, clearly
demonstrating that the pyramidal tract can modulate
activities of the sensory relay nuclei. Andersen et al.
(6) showed that cortical stimulation could evoke de-
polarization of primary afferent fibers in the cat, and
Fetz (47), using the same species, demonstrated that
at least a part of the depolarization was mediated by
the pyramidal tract. The latter investigator also dem-
onstrated that pyramidal tract stimulation could ex-
cite or inhibit neurons in the dorsal horn. From these
experiments it has become clear that some pyramidal
tract neurons can influence the activities of various
subcortical motor nuclei or sensory relay nuclei. Fur-
thermore, Zarzecki et al. (165) have shown that some
pyramidal tract cells in area 3a (63) send long axon
collaterals to the motor cortex. Yet there are demon-
strations that some corticofugal neurons projecting to
the ventrolateral nucleus (23) and the dorsal column
nuclei (57) do not project to the spinal cord. Anatomic
studies with horseradish peroxidase have revealed that
cortical cells projecting to the corpus striatum are
located in the superficial part of layer VI and also in
the deeper part oflayer V in the monkey (76), whereas
the majority of corticocaudate projection cells are
located in layer III in the cat (81). Thus the results
are still controversial, but it seems that at least some
pyramidal tract fibers give off collaterals before reach-
ing the medullary pyramid and send branches to var-
ious subcortical nuclei. The functional significance of
these collateral branches are still unknown, but it may
be said that activities of the pyramidal system are
accompanied by corollary activities of the sensory and
other motor systems to produce purposeful move-
ments.
AFFERENT INPUTS TO MOTOR CORTEX
AND PYRAMIDAL TRACT NEURONS
General Problems
Inputs to the motor cortex have been studied less
extensively than the outputs from the motor cortex,
and they have been studied more anatomically than
physiologically. Various methods, each with its own
limitations, have been used to determine the connec-
tions. It is generally agreed that the motor cortex
receives its main inputs from the thalamus. It also
receives projections from the ipsilateral hemisphere
through association fibers and from the contralateral
hemisphere through commissural fibers. Recent de-
velopments in autoradiography and horseradish per-
oxidase techniques have made it possible to study
further details of projections from various areas, and
our knowledge is increasing rapidly.
Inputs From Nucleus Ventralis
Lateralis of Thalamus
The motor cortex receives its major inputs from the
nucleus ventralis lateralis of the thalamus. Olszewski

(120) subdivided this nucleus into three main parts:
pars oralis, pars medialis, and pars caudalis in the
monkey. The largest subdivision is the pars oralis, and
it receives fiber connections from the cerebellar nuclei
and the globus pallidus. The pars medialis receives
fibers from the globus pallidus and the substantia
nigra. Corticofugal fibers from the precentral cortex
project to the pars oralis and the pars caudalis, con-
stituting reciprocal connections between the nucleus
ventralis lateralis and the cortex. It has been suggested
that there is a crude topographic organization within
the nucleus ventralis lateralis (157). Medial parts of
the nucleus send fibers to the face area, intermediate
parts to the arm and trunk area, and lateral parts to
the leg area of the cortex. Using the Fink-Heimer
method, Strick (142) studied the distribution of degen-
erating fibers from small regions of the nucleus ven-
tralis lateralis in the cat. He confirmed the existence
of crude topographic projection to the motor cortex,
and reported that the projection from a small area of
the nucleus ventralis lateralis was not restricted to a
small area of the motor cortex. A small lesion in the
nucleus ventralis lateralis produced sparse degenera-
tion spread over a relatively wide area of the motor
cortex. Larger lesions increased the density of degen-
eration within the same cortical area, indicating an
extensive arborization of individual ventrolateral fi-
bers in the motor cortex. Massion and Rispal-Padel
(108) examined the projection from nucleus ventralis
lateralis in cats using physiological methods. They
implanted several (12-16) stimulating electrodes into
the depths of the motor cortex and examined the
distribution of neurons in the nucleus ventralis later-
alis activated antidromically from the individual elec-
trodes. They also confirmed the existence of topo-
graphical relationships between the motor cortex and
the nucleus ventralis lateralis and in addition found
that some ventrolateral neurons (8 of 29) could be
activated from more than one cortical stimulating site,
clearly indicating that some neurons send branches to
different parts of the motor cortex. Because the num-
ber of the cortical electrodes was limited, it is likely
that the actual ratio of the neurons with bifurcating
axons is higher than they had observed. Subsequently
Asanuma and Fernandez, in collaboration with Schei-
bel and Scheibel (19), studied the characteristics of
these projections in cats using physiological and ana-
tomic methods. They found that each terminal bush
of these multiple branching neurons covers a much
wider area than that covered by the specific projection
fibers originating from the thalamic sensory relay nu-
clei and project to their respective sensory cortices
(99). Scheibel and Scheibel (19) were able to stain
these terminal bushes of young cats using the Golgi
method (Fig. 17). The width of these terminal bushes
measured in the horizontal direction was 1.16 ± 0.27
mm in diameter, and the terminal fibers reached to
the upper part of the second cortical layer. The pre-
dominantly oblique direction of the components of the
CHAPTER 15: THE PYRAMIDAL TRACT 719
250 u
FIG. 17. Terminal intracortical domain generated by axon of
single thalamic ventrolateral neuron shown in relation to large fifth-
layer pyramidal neuron. g, Gray matter-white matter junction.
Reconstruction at lower left shows single ventrolateral fiber system
projecting onto pericruciate gyrus, pc. Two of these tridimensional
plexuses are shown developing from same fiber via branch point, b;
young kitten cortex. c, Cruciate sulcus; m, medial; 1, lateral. [From
Scheibel and Scheibel, in Asanuma et al. (19).]
axonal plexus in the lower two-thirds of the terminal
arbor suggested that contacts were most likely made
with some of the basal dendrites of pyramidal cells
and with some of the oblique branches of the apical
shafts. The majority of terminal branches were located
in the superficial layers, which suggested that they
might have synaptic contacts with or climb along the
apical dendrites of large- and medium-sized pyramids.
Strick and Sterling (148) examined synaptic termina-
tions of afferent fibers from the ventrolateral nucleus
in cats using light microscopy and electron micros-
copy. They reported that following the ventrolateral
lesion, degenerating synapses were mainly found in
three layers: the upper one-third oflayer I (18%), layer
III (66%), and layer VI (13%). Some of the synapses
were found on the dendritic shafts or cell bodies of
stellate cells, but most (91%) were found on the den-
dritic spines. Because it is known that ventrolateral
stimulation produces mono- and polysynaptic activa-
tion of pyramidal tract cells (5), it is likely that some
of these degenerating fibers made synapses on the
dendritic spines of pyramidal tract cells.
The nature of the afferent inputs to ventrolateral
neurons has been studied repeatedly (19, 106, 107),
and all the investigators agree that these neurons do
not receive specific peripheral inputs. This excludes
the possibility that receptive fields of neurons in the
motor cortex are transferred through ventrolateral
neurons. Activities of neurons in the nucleus ventralis
lateralis during natural movements were studied by
720 HANDBOOK OF PHYSIOLOGY - THE NERVOUS SYSTEM II
Evarts (43) and Strick (144) in the monkey. They
found that some ventrolateral neurons discharged
prior to movements, suggesting that they were related
to the initiation of movements. Unlike many motor
cortex neurons that receive peripheral inputs, how-
ever, most of them were not influenced by natural
stimulation in the periphery.
Peripheral Inputs to Motor Cortex
and Pyramidal Tract Cells
During the several decades following the discovery
of the motor representation within the cortex (53), the
major interest among neurologists and neurophysiol-
ogists was the localization of motor function; little
attention was paid to the sensory inputs to the precen-
tral cortex (124). With the advancement of electrical
techniques, Adrian and Moruzzi (1) were able to record
discharges in the pyramidal tract in response to pe-
ripheral stimulation, which clearly demonstrated that
pyramidal tract cells received peripheral inputs. As
already stated, Woolsey and his collaborators (163)
studied the distribution of evoked potentials in both
the sensory and motor cortices in combination with
stimulation of the cortex, and they reported that there
were rough topographical relationships between affer-
ent input and efferent outflow. They observed that
the area of the motor cortex where the largest evoked
potential was recorded by stimulation of a particular
part of the body had the lowest threshold for the
movement of the same part of the body. Following the
development of the microelectrode technique, the na-
ture of the inputs was studied extensively. In the early
stage of these experiments, however, the results were
confusing. The experiments were frequently carried
out under chloralose anesthesia using electrical stim-
ulation instead of with unanesthetized animals and
natural stimulation. Under the former conditions, mo-
tor and sensory cortical cells received widespread con-
vergence of inputs without recognizable patterns of
spatial localization or sensory modality. Most cells
responded to electrical stimulation applied to any part
of the body (153). It was noticed later that chloralose
enhances the activity of the nonspecific system (2).
These widespread responses could therefore have been
produced by abnormal activities of the system.
The receptive fields of neurons in the motor cortex
were studied extensively with cats by Brooks et al. (27,
28) and by Buser and Imbert (32). The experiments
were carried out under local anesthesia with natural
stimulation. These authors found that the pattern
of sensory activation was similar in pyramidal tract
and nonpyramidal tract cells. About 65% of cells re-
sponded to cutaneous stimulation, 20% to passive joint
movement, and the remainders were not driven. More
than one-half of driven cells received modality-specific
inputs from a fixed small area of the body. The rest
received inputs from wide areas of the body, and some
of these had labile receptive fields. In a subsequent
study by Welt et al. with cats (159), it was found that
cells with similar receptive fields were grouped to-
gether in a small area of the cortex. These cells were
intermixed with other groups of cells that received
inputs of different modalities but that had receptive
fields located in the same area of the body. These
groups of cells were located in a small area extended
along the direction of radial fibers in the cortex, and
their diameters ranged from 0.1 mm to 0.4 mm. An
example of these aggregates of cells is shown in Figure
18.
A natural question following these observations is
whether a group of afferent inputs converging from a
particular part of the body to a small area of the cortex
is related to the motor function of the cortex. The
problem has been studied by Asanuma and his collab-
orators in cats (18) and monkeys (133) using a closed-
chamber system that allowed recordings from single
cortical neurons while animals were awake and able
to move. The receptive fields of neurons were exam-
ined first, then the same electrode was used to stimu-
late these neurons and their neighbors to produce
contraction of individual limb muscles. It was then
possible to relate the afferent inputs to a small area of
the cortex with the motor effects elicited from the
same area. They found that a given efferent zone
received polymodal inputs from skin as well as from
deep structures. Figure 19 shows an example of the
results in the cat. The cutaneous receptive fields of
neurons in a given efferent zone were spread over a
relatively wide area surrounding the target muscle,
but most of them were located on a skin region that
lay in the path of the limb movement produced by
contraction of the target muscle. The inputs from the
deep structures arose mostly from the joint where the
target muscle was inserted (18). This input-output
relationship is more elaborate in the monkey motor
cortex (133). As illustrated in Figure 10, cortical effer-
ent zones that produced contraction of individual mus-
cles were located along the direction of radial fibers
within the depth of the motor cortex. While delineat-
ing these efferent zones, Rosen and Asanuma (133)
examined the peripheral inputs to neurons in each
efferent zone. As in the cat, a single zone received
various inputs arising from deep as well as superficial
receptors. Figure 20 illustrates the input-output rela-
tions of cortical efferent zones in a sagittal row of
penetrations through the thumb area of the cortex. In
addition to passive movements of thumb, two cells in
the thumb flexion zone responded to touch of the skin,
and the receptive fields of both cells were on the
ventral aspect of the thumb. The cells in the zones
producing extension, adduction, and abduction of the
thumb were activated by touch of the distal tip, medial
surface, and lateral surface of the thumb, respectively.
The characteristics of this input-output relationship
suggested that each zone received afferent inputs re-
lated to movement produced by the activity of the
same zone, because the receptors were located in the
 CHAPTER 15: THE PYRAMIDAL TRACT 721

DEEP SUPERFICIAL
PRESSURE. ~~TOUCH
PROTRACTION __ HAIR

::)
A

~
:~-
~
::J
c

... PT-CELL
• NON-PT
o NOTTESTED
FIG. HI. Example of multimodal sensory inputs from small area in periphery to cortical column in
cat. A: location of penetration on pericruciate cortex. Dotted line indicates sagittal plane of section.
B: diagram of sagittal section and of radial penetration in gray matter. C: photomicrograph of part of
section containing penetration. Figurines show peripheral receptive fields. Adequate stimuli to deep
structures shown at left and those to the superficial structure shown at right. [From Welt et al. (159).]

region that tended to be stimulated by contraction of
the target muscle. From these experiments in cats and
monkeys, it was concluded that a cortical efferent zone
receives feedback information related to the contrac-
tion of the target muscle.
Lemon et al. (93,95) studied the input-output rela-
tionship with a different approach, using awake mon-
keys. They recorded activities of precentral neurons
while the monkey performed a wide variety of move-
ments in order to collect a food reward placed in a
number of different positions. They selected those
neurons that showed definite modulation of their dis-
charge frequency related to specific movements about
one joint and then examined receptive fields of these
neurons by natural stimulation. They reported that
the majority of neurons examined received afferent
inputs from areas that were anatomically closely re-
lated to the joint involved in the movement with which
the discharges of the neuron were modulated. These
results are in agreement with those obtained using
microstimulation methods (133), but Lemon et al. (93,
95) also reported that not all the members of a re-
stricted local population shared the same peripheral
territory. These latter results may contradict the pre-
vious study (133) in which neurons in a given efferent
zone received inputs related to the movements pro-
duced by microstimulation of the same zone. This
problem was restudied by Murphy and his collabora-
722 HANDBOOK OF PHYSIOLOGY - THE NERVOUS SYSTEM II

G POSTCRUCIATUS

8•

.... .
'
........

1mm
FIG. 19. Afferent inputs converging into cortical efferent zone for palmar muscle. Of 8 penetrations,
4 passed through palmar zone, and 17 cells could be isolated within the zone. Six of 17 cells responded
to natural stimulation of skin; receptive fields shown by figurines connected to cell locations by
respective lines interrupted by penetration and cell number. These 6 neurons shared common
receptive field on ventral surface of paw. [From Asanuma et al. (18).]

tors (115) using awake monkeys and the microstimu-
lation technique. They studied the same monkey over
a period of 18 mo and made a detailed map of cortical
efferent zones in relation to their afferent inputs. They
confIrmed the results of Rosen and Asanuma (133)
and concluded that the results of Lemon et al. (93)
could occur if penetrations were made in the boundary
areas of adjacent zones or if they were made in a
direction parallel to the cortical surface in the sulcus,
which would sequentially traverse several vertical ag-
gregates representing different limb joints. Murphy et
al. (115), however, also reported that when neurons
received cutaneous inputs the movements induced by
microstimulation of the same sites were, in about one-
half of the cases, in the direction which withdrew the
limb away from the loci of adequate peripheral stimuli.
These results were somewhat contradictory to the
previous results, because Rosen and Asanuma (133)
reported that cells activated by tactile stimuli had
receptive fIelds almost exclusively on the glabrous
volar surface of the hand and lay within cortical effer-
ent zones projecting to fInger flexor muscles. The
controversy might have stemmed from the following
differences. In their study, Rosen and Asanuma (133)
restricted the stimulating current to 10 !LA or less
because current beyond this range frequently pro-
duced complicated fInger movements, making analysis
of the results difficult. Because the thresholds for
contraction of proximal limb muscles were higher,
their study was restricted to areas that induced move-
ment ofthe hand and fIngers. Murphy et al. (115) used
stronger current of up to 30 !LA and examined input-
output relationships not only in the distal, but also in
the proximal limb area. These zones from which move-
 CHAPTER 15: THE PYRAMIDAL TRACT 723

..
'

5 10····· 15
.'
..
'

I
.....................

'. j.. ..1

.\•••• '. ·······UD
I
...... .....
.....' ····un
un'" 1\' III' 1111

UD······
......'
'
\UD

............
. ------ I Thumb e"ten.lon

----
Thumb
••••.'
UD

.......
.. ' un
D
o
E"t
Flex
UD Thumb extension
........ • Add

...:....' • Abd

"
.........
",'

FIG. 20. Afferent inputs converging to thumb area of monkey motor cortex. Several penetrations
passed through areas, which when stimulated produced extension, flexion, adduction, or abduction of
thumb. Each area marked by symbols explained at lower right. Cortical sites from which movement
could not be produced are shown by small bars on electrode tracks. Locations of isolated cells are
indicated by dots, and are connected to descriptions of receptive fields and adequate stimuli by dotted
lines. Filled areas on figurines are superficial receptive fields. UD, undriven cells. [From Rosen and
Asanuma (133).]

ments were induced away from the peripheral recep-
tive fields were located in the rostral part of the motor
cortex and represented proximal limb muscles where
cutaneous inputs have not been reported by previous
investigations (133,93). In the results of Murphy et al.
obtained from the area near the central sulcus, how-
ever, the relationship was the same as that reported
by the previous investigators (133). This seems to
suggest that the input-output relationship in the prox-
imallimb area is more variable than that in the distal
limb area.
In their study, Rosen and Asanuma (133) recorded
from a total of 192 cells, and about one-half (45%)
responded to peripheral stimulation. The distribution
of these responsive cells was not uniform within the
motor cortex, however. As already described, not all
areas of the motor cortex, even in the distal limb area,
produced contraction of muscles with intracortical
microstimulation of limited intensity. The low-thresh-
old efferent zones (10 J.LA or less) were clustered in
some parts of the motor cortex constituting an over-
lapping mosaic, and in other parts the zones were
scattered with intercalating silent areas. Peripheral
afferent inputs projected more heavily into the low-
threshold zones. In the efferent zones 52% of all iso-
lated cells responded to peripheral stimulation,
whereas in the silent areas (threshold> 10 J.LA) only
32% responded. Although an increase in the stimulus
intensity delivered within a silent area could produce
muscle contractions, the effect then tended to appear
in more than one muscle and the input-output rela-
tionship became less clear, even in the distal limb area
(133).
Asanuma et al. (19, 133) did not identify the recep-
tors located in the muscle. The identity of these recep-
tors has been studied by Murphy et al. (116, 117) using
locally anesthetized cats. They denervated the fore-
limb except for those nerves innervating the extensor
724 HANDBOOK OF PHYSIOLOGY - THE NERVOUS SYSTEM II

digitorum communis muscle and the flexor palmaris peripherally evoked potentials in the monkey motor
longus muscle. After fixation of the elbow joint, the cortex after removal of the sensory cortex. In the cat,
distal tendons of these muscles were severed, and the Thompson et al. (152) reported that receptive fields of
muscles were stretched by pulling the tendons. Mur- neurons in the motor cortex did not change before and
phy et al. observed that neurons in the motor cortex during the cooling of the sensory cortex. The nucleus
responded to both low-velocity stretches, which acti- ventralis posterolateralis of the thalamus, which relays
vate primary endings of muscle spindles, and high- peripheral inputs to the sensory cortex, does not pro-
velocity stretches, which principally activate second- ject to the motor cortex, and the nucleus ventralis
ary spindle endings and Golgi tendon organs. Because lateralis, which sends the major inputs to the motor
they combined intracortical microstimulation with cortex, does not receive peripheral inputs in either
these recordings, they were able to relate the location cats (19, 106, 107) or monkeys (144). Hence the path-
of these neurons to the cortical efferent zones. They way for direct inputs to the motor cortex was uncer-
found that neurons showing threshold responses to tain. Recent development of horseradish peroxidase
low-velocity stretches were located exclusively within technique made it possible to reveal finer features of
the cortical efferent zones that projected to the same projection than were revealed by the degeneration
muscle. Neurons responding to high-velocity stretches methods. It has been shown in both cats (88) and
were found not only in the same zone, but also- monkeys (143) that a small area between the ventralis
although sparsely-outside of the zone. The results lateralis and ventralis posterolateralis [(pars oralis of
revealed that the cortical efferent zones receive pe- ventralis posterolateralis of Olszewski; (77)] sends fi-
ripheral inputs not only from receptors in the skin, bers directly to the motor cortex. Subsequently the
joint, and connective tissues, but also from those lo- physiological properties of neurons in this border area
cated in the muscle itself. have been studied in both cats (14) and monkeys (15,
94). In these experiments the thalamic projection neu-
PATHWAYS FROM PERIPHERY TO MOTOR CORTEX. Until rons were antidromically activated from the motor
recently it has been controversial as to whether the cortex and then the receptive fields of these identified
motor cortex receives peripheral inputs directly from neurons were examined. In both species, neurons in
the thalamus or only via the sensory cortex (160). the border area between the ventralis lateralis and
There were observations that indicated that some of ventralis posterolateralis received somesthetic inputs
the inputs from the periphery arrive at the motor similar to those received by neurons in the motor
cortex directly from the thalamus. Using evoked po- cortex. In the example shown in Figure 21, 56 neurons
tential methods, Malis et al. (104) were able to record were isolated, and 3 of them were activated antidrom-

A C
1 2 3 4
~~~c:::o
::=:i} ~ E=CD ID==
FIG. 21. Thalamic neurons that transfer periph-
eral somesthetic inputs directly to motor cortex in
cat. A: sagittal section of ventral thalamus showing
electrode tracks and lesions. B: reconstruction of
=:1l =:§ (CO) (CJ
tracks from histological preparations. Short bars ~~ID=
on tracks show locations of neurons with no recep-
tive fields. Long bars at right are locations of ~«t=
neurons activated from skin receptors. Long bars :Q.':ll~
at left are those activated from deep receptors.
Circles indicate lesions made during experiment.
Arrows indicate neurons activated antidromically
from motor cortex. C: receptive fields of neurons
B ~~
~~
shown in B. Solid areas indicate receptive fields ,---~--'T-----"'".--T-------,-"" ~~
for hair bending or light touch. Circles indicate
deep receptive fields such as pressure or passive ~
joint movement. Numbers on column correspond
to track numbers, and each figurine corresponds to
=o:::J
respective long bar on the track. [From Asanuma ~
et al. (14).]
ib?
=d3
~
~~
===:§
 CHAPTER 15: THE PYRAMIDAL TRACT 725

ically from the motor cortex. Of these 3, 2 were acti- Motor ex

vated by passive movement of joints. Of 40 cells pro-
jecting to the motor cortex from the border area, 12
received inputs from the skin, 20 from deep structures,
and 8 were undriven from the periphery. Furthermore
it has also been shown that ablation of the sensory
cortex does not significantly change the characteristics
of the receptive field of neurons in the motor cortex in
either cats (14) or monkeys (15). It was concluded that
at least some of the peripheral somesthetic inputs
arrived in the motor cortex directly from the thalamus
without passing through the sensory cortex in both
cats and monkeys (15).
Pathways conveying the inputs to the motor cortex
were studied by making lesions in the spinal cord.
Asanuma et al. (17) reported that in the cat the
amplitudes of potentials evoked in the motor cortex
by stimulation of either skin or muscle afferents were
reduced by section of the spinocervical tract or dorsal
column. In the monkey (16), section of the dorsal
column abolished the evoked potentials in the motor
cortex, but spinothalamic tract section reduced the
amplitude of the potentials only in the sensory cortex.
Brinkman et al. (24) observed that the receptive fields
of neurons in the monkey motor cortex disappeared
almost completely after dorsal column lesions. From
the above experiments it became clear that the dorsal
column plays the major role in transferring peripheral
inputs to the motor cortex in the monkey, whereas FIG. 22. Simplified diagram of connections between motor cortex
both spinocervical tract and dorsal column are in- (motor Cx) and periphery. Neurons in motor cortex are connected
volved in the cat. predominantly in radial direction and are subdivided into cortical
The simplest connections between the motor cortex efferent zones marked by hatched and dotted areas. Fringes of these
efferent zones overlap with fringes of others, constituting overlap-
and the periphery are shown diagrammatically in Fig- ping mosaic within cortex. These efferent zones are intercalated
ure 22. This diagram is meant to illustrate only a part with silent areas where threshold for motor effect is high. Cortico-
of the connections between the cortex and the periph- spinal fibers from given efferent zone project most heavily to given
ery. Pathways are shown by which cortically induced motor nuclei to produce contraction of a muscle, but they also
project to other motor nuclei to produce subliminal fringes of
movements send peripheral information directly back excitation. Afferent inputs originated by contraction of target mus-
to the original cortical areas continuously during cle ascend spinal cord and project to original efferent zone directly
movements. through nucleus ventralis pars oralis, constituting a closed loop
between cortex and periphery. This corticoperipheralloop circuit is
FUNCTIONAL SIGNIFICANCE OF PERIPHERAL INPUTS TO well developed for distal limb muscles but is less clear for proximal
MOTOR CORTEX. It has been shown that voluntary muscles.
movement is severely disturbed by interrupting inputs
from the periphery. Mott and Sherrington (112) re- animals the reflexes in which the motor cortex is
ported that deafferentation of the upper limb resulted known to participate are the placing (21) and grasping
in a loss of the use of the hand, closely resembling the (37) reactions. Both reactions can be elicited by tactile
symptoms that follow ablation of the motor cortex, stimulation of a part of a limb. Although it is possible
although the responses to electrical stimulation of the that the peripheral inputs arriving directly at the
cortex were not impaired. This experiment was re- motor cortex play some role in these reflexes, it is
peated by many investigators, and it was found that unlikely that they play a major role. Both reflexes
the loss of the movement is not permanent. It became persist as long as sensory and motor cortices are intact,
clear that in certain circumstances the monkey can but disappear after either the sensory or the motor
eventually ambulate with the deafferented arm and cortex is removed, whereas the peripheral inputs to
can also learn to reach for food using visual guidance, the motor cortex persist after ablation of the sensory
although the movement is not as smooth as in the cortex. Furthermore it has been shown recently in the
normal animal (82). These observations demonstrate kitten (52) that the tactile placing reaction persisted
the importance of afferent inputs for voluntary move- in the hindlimb after transection to the spinal cord at
ments, but the role of afferent inputs arriving directly the level of the first lumbar segment. Amassian (3)
at the motor cortex is still in question. In normal reported that in the kitten tactile placing was sub-
726 HANDBOOK OF PHYSIOLOGY - THE NERVOUS SYSTEM II
served by a subcortical circuit, and the subsequent
involvement of the cerebral cortex started to occur
through tonic rather than dynamic activity. The re-
sults suggest that tactile placing is a subcortical or
even a spinal reflex. As the tactile placing reaction
disappears with pyramidal section in adult monkeys
(154), the role of the pyramidal tract in the adult
monkey may be to modulate the activity of subcortical
circuits. These circuits may be activated not by the
direct inputs to the motor cortex, but by the inputs to
the sensory cortex, which are then relayed to the
motor cortex via corticocortical and/or subcortical
pathways.
It was proposed that the direct sensory inputs to the
motor cortex function as positive feedback information
related to movements (15). As the type of inputs to
the cortex and the nature of efferent projection to the
muscle indicate the existence of loop circuits between
the motor cortex and the periphery, it is possible that
impulses circulate within a set of circuits during a
particular movement. This circulation of the impulses
could result in an increase of the excitability of efferent
and afferent relay nuclei involved in these circuits and
subsequently further increase the excitability of re-
lated cortical efferent zones. Such an increased excit-
ability of these loop circuits including the cortical
efferent zones could alter the efficacy of excitatory and
inhibitory inputs from other pathways. Because the
motor cortex is known to be involved in multiple-loop
circuits with various sites in the central nervous sys-
tem, such as other areas of the cerebral cortex, sub-
cortical nuclei, and cerebellum, there is the possibility
for an interaction of these circuits, including the one
between the cortex and the periphery, in the produc-
tion of various combinations of muscle contractions
during normal movements.
Inputs Through Association Fibers
The existence of interconnections between various
parts of the cortex has been known for a long time,
but detailed studies were made after the introduction
of the Nauta method (118). The development of au-
toradiography and horseradish peroxidase methods
have made it possible to reveal yet a finer structure of
the connections between various areas, and these stud-
ies are progressing rapidly. Stimulated by these find-
ings, physiological experiments are also vigorously
being carried out. The following section describes the
recent information concerning the fine connections
between the motor cortex and other areas of the
cortex.
INPUTS FROM SENSORY CORTEX. The connections be-
tween the motor and the sensory cortices have been
studied extensively. Using the Nauta method, Jones
and Powell (78, 80) studied these connections in the
cat and the monkey. They found that in both species
the first and second somatic sensory area and the
motor cortex are all reciprocally interconnected by
association fibers. Physiological studies in the monkey
have revealed that different areas of the primary sen-
sory cortex receive different inputs from the periphery.
Areas 1 and 2 receive inputs primarily from receptors
located in deep structures such as those excited by
rotation of or pressure on joints, whereas area 3b
receives inputs from receptors in the skin (129). In
both cats and monkeys, neurons in area 3a receive
inputs primarily from group I muscle afferent fibers
(4, 121, 128). Projections from these subdivisions of
the sensory cortex to the motor cortex have been
studied subsequently. Grant et al. (58), using cats,
made a needle-stitch lesion in area 3a where the max-
imal group I-evoked potential was recorded. They
found that degenerating U-fibers originating from the
lesion traveled in the white matter to the cortex of
areas 4y, 3b, and 2. These fibers branched in layer III,
and some of them reached layer I. The degenerated
fibers were distributed as distinct columns with a
diameter of about 1 mm, the same diameter as the
cortical efferent zones in the motor cortex. Zarzecki et
al. (164), using anesthetized cats, studied the physio-
logical properties of projection neurons in area 3a,
which were identified by their antidromic activation
from the motor cortex (area 4y). They showed that
most of the projection neurons were located in layer
III, with some in layer V. By recording intracellularly
from those neurons, they were able to demonstrate
strong excitatory synaptic inputs from group I affer-
ents. The information transferred by these cortico-
cortical fibers may contribute to the formation of
receptive fields of neurons in the motor cortex, but it
probably does not playa major role because cooling
area 3a does not abolish inputs from a specific muscle
to neurons in a given efferent zone (116).
Theories concerning the functional significance of
this projection are still controversial. One of the sug-
gested functions has been a participation in cortical
regulation of muscle contraction. It has been shown
that the sudden extension of the forearm of a human
subject could evoke two separate bursts of electro-
myographic activity in the biceps muscle (62). The
first was identified as the tendon jerk by its short
latency. The second burst had a latency of about 50
ms, and the magnitude of this component increased
when the subject resisted the tension and decreased
when he was told to "let go" (61). This second burst
was termed "function stretch reflex" (109), and Mars-
den et al. (105) suggested that this reflex might serve
to counteract unexpected loads encountered in the
course of a willed movement. They proposed that this
reflex was mediated by a relatively simple transcortical
loop. Several studies have been carried out to clarify
the role of sensory and motor cortices in this reflex
using chronically trained monkeys (42,44, 151). It was
shown later (56), however, that the two separate bursts
of electromyographic activity persisted in decerebrate
and spinal cats. These results indicate that the second
burst does not necessitate the transcortical loop that

carries group I muscle afferents. One possibility is that
the cortex influences the functional stretch reflex by
tonically changing the excitability of the lower centers.
Another suggestion has been made by Phillips (127)
based on the following evidence. Foerster (51) reported
that rhizotomy performed on patients with intractable
pain impaired most severely the manipulation of in-
dividual fingers, although the patients could move
their arms and hands. On the other hand, Merton
(110) reported that deprivation of all inputs other than
the spindle feedback did not impair the movement of
the thumb in a normal subject. In this experiment a
sphygmomanometer cuff was kept inflated at the wrist
until all sensation was lost from the hand. Skin and
joints and intrinsic hand muscles were thus reversibly
denervated, but the spindle feedback from the long
flexors and extensors of the fingers remained intact.
In this condition the subject was still able to move his
thumb voluntarily and even to move a pointer at-
tached to it through a prescribed angle. Eklund and
Hagbarth (38) reported the following experiments. A
normal subject was instructed to try to maintain a
steady isometric force, flexing the elbow against a
restraining strain-gauge dynamometer at the wrist.
When the biceps tendon was vibrated, there was a
large increase in force of which the subject was quite
unaware. As longitudinal vibration is a highly selective
stimulus to the primary endings of the muscle spindles
(29), it is likely that the artificially disturbed spindle
feedback provided the wrong information. Based on
these evidences and on the results of his group (87)
that colonies of corticomotoneuronal neurons have a
direct and powerful connection with the motoneurons
innervating the hand muscles in the baboon, Phillips
(127) proposed that inputs from muscle spindles to the
cortex may function as part of a transcortical servo
loop that signals the discrepancy between intended
and actual movements.
Jones et al. (77), using anterograde and retrograde
transport methods, and Vogt and Pandya (156), using
a degeneration method, have more detailed studies of
projections from the somatic sensory areas in the
monkey. Both groups reported that area 3b, which is
known to receive inputs primarily from skin receptors,
did not project to the motor cortex but projected to
areas 1 and 2. Area 1 was reciprocally connected to
area 3 but sent the strongest projection to area 2, and
area 2 was reciprocally connected to the motor cortex.
Neurons in area 2 receive inputs predominantly from
receptors in deep structures (129) in the monkey, and
it is possible that area 2 transfers these inputs to the
motor cortex. It is also known, however, that in the
monkey, receptive fields of neurons in the motor cortex
do not change significantly after removal of the sen-
sory cortex, including area 2 (15). In addition the
virtual absence of projection from areas 3b and 1 to
the motor cortex makes it unlikely that corticocortical
projections play an important role in forming cuta-
neous receptive fields of neurons in the motor cortex.
CHAPTER 15: THE PYRAMIDAL TRACT 727
INPUTS FROM ASSOCIATION CORTEX. Strick and Kim
(146), using the horseradish peroxidase method, and
Zarzecki et al. (165), using physiological methods,
demonstrated that there was a rather heavy projection
from area 5 to area 4 in the monkey, and that the
projection was topographically arranged. It has been
reported by Mountcastle et al. (114) that some neurons
in areas 5 and 7 of the monkey cortex were not
activated by sensory stimuli but were discharged at
high rates when the animal moved its arm to obtain
an object. They proposed that these neurons function
in a command fashion, directing visual attention to
and the exploration of the immediately surrounding
extrapersonal space. The strong connection between
area 5 and the motor cortex suggests a functional
coupling between the two areas, but whether or not
this connection plays an important role in the com-
mand of movement, which is a complex function, is
still in question.
Inputs Through Commissural Fibers
Much is known about the commissural connections
for the visual and association cortices, but few studies
have been carried out concerning the connections
between the motor cortices. Using cats, Asanuma and
Okuda (19) reported that orthodromic excitation of
pyramidal tract cells could be evoked from a circum-
scribed area of the contralateral cortex. The excitatory
point was surrounded by an area, the stimulation of
which inhibited the discharges that were evoked from
the center. The results suggested the existence of
topographic projections between cortices with a gen-
eral feature of an on-center, off-periphery arrange-
ment. This, however, does not seem to be the general
scheme of connection between the motor cortices,
because it was later found in the monkey (122) that
although axial and limb girdle areas of the precentral
areas are mutually interconnected, the neurons in the
hand and foot areas do not project to the contralateral
cortex. There is a somewhat similar arrangement in
the somatosensory area in the cat in which the callosal
connections are limited to areas representing the face,
trunk, and limb girdles (79). These results are inter-
esting because they suggest that distal limb areas
controlling the fine movements of limbs are mutually
independent, which may be important for the produc-
tion of a variety of combinations of independent limb
movements.
FUNCTION OF PYRAMIDAL TRACT
The traditional methods of studying the functions
of the central nervous system are to stimulate or
ablate a part of the system and to observe the effects.
Stimulation experiments were dealt with in the pre-
ceding sections, and only ablation experiments are
described in this section. A new method introduced
recently in which activities of individual neurons are
728 HANDBOOK OF PHYSIOLOGY - THE NERVOUS SYSTEM II
studied in relation to trained movements of the animal
(41) are not discussed here. The results from this latter
type of experiment are described fully in the chapter
by Evarts in this Handbook.
To study the genesis of the symptoms of hemiplegia
has been one of the most intriguing challenges to the
neurologist and neurophysiologist. Hemiplegia, caused
by damage to the internal capsule, is typified by pa-
ralysis with spasticity. It is accompanied by exagger-
ated deep tendon reflexes, the Babinski sign, and
absence of abdominal and cremasteric reflexes. All of
these symptoms were once thought to be caused by a
lesion of the pyramidal tract. Accumulation of careful
clinical observations had cast some doubt on this
interpretation, although the controversy continued as
to whether the lesion of the pyramidal tract contrib-
uted to the spasticity of the muscles. It was Tower
(154) who clearly demonstrated that a pyramidal le-
sion did not produce spastic paralysis. The main defi-
cits after pyramidal section were diminished muscle
tone, diminished cutaneous reflexes, slow tendon re-
flexes restricted to the stimulated muscle, and defec-
tive initiation and execution of all performance by
skeletal musculature, particularly the loss of all dis-
crete usage of digits. The tactile placing reaction was
lost permanently, but a Babinski sign did not develop
although it was later shown that the Babinski sign
could develop in the chimpanzee after pyramidal sec-
tion (69). Tower summarized pyramidal functions in
space and time as follows: "The spatial function is the
ability to bring into action any portion of the skeletal
muscui", ure, and in all combinations. This detailed
control of the skeletal musculature enables the dis-
crete usage of musculature, especially of the digits,
and the modulation of extrapyramidal activity, which
are outstanding pyramidal functions. In time, the py-
ramidal tract operates in two phases. One is a contin-
uous, or tonic, action in effect at all times in the
waking state. The other is a specifically timed increase
of discharge, or phasic action, which is evoked in
relation to particular situations." She concluded that
"together, the tonic function provides for smooth,
continuous, efficient action while the phasic function
contributes, outstandingly, precision and lability to
total performance."
The pioneering work of Tower has been repeated,
and the results have been confirmed by many inves-
tigators, but there were some controversies. One of the
problems was whether or not the loss of control of fine
movements was permanent. Bucy et al. (30) cut the
cerebral peduncles bilaterally, although not always
completely. They observed that some of the fully
recovered animals were able to use the thumb and
index finger along to pick up food, although others
could not. The difficulty in these experiments was
determining the extent of the pyramidal section. Law-
rence and Kuypers (92) argued that the recovery was
caused by incomplete section of the pyramidal tract.
They interrupted the pyramidal tract bilaterally in 39
monkeys, and in 8 of them the lesion was virtually
limited to the pyramidal tracts. These animals could
sit with head up and could stand, walk, run, and climb
immediately following the operation. They soon re-
gained the capacity for independent use of their ex-
tremities, and within 3 wk they could reach accurately
with either hand to pick up morsels of food by closure
of all fingers in concert. Individual finger movements
never returned, however, even after recovery periods
of up to 11 mo. In addition all movements were slower,
and the monkeys fatigued more rapidly than normal
animals. These results virtually confirmed the obser-
vations reported by Tower, except for their emphasis
that pyramidal deficits were more restricted to the
manipulation of distal extremities. Using the monkey,
Hepp-Reymond and Wiesendanger (64) and Hepp-
Reymond et al. (65) examined the effect of pyramidal
section on the reaction time and force exerted during
precision tasks. The monkeys were trained to squeeze
a transducer between the thumb and index finger and
were tested before and after unilateral or bilateral
pyramidotomy. After partial pyramidotomy there was
a long-lasting slowing in the performance of the finger
grip. This delay was due not only to weakness of the
muscle contraction, but also to delay in the initiation
of the movement. These results partially conflict with
the results reported by Laursen and Wiesendanger
(91) on cats and Laursen (90) on monkeys. In both of
these experiments, the animal was trained to react to
the test stimulus in different fashions, depending on
the conditioning stimulus. After partial pyramidotomy
it was found that the reaction time was increased
when a choice was involved but not when discrimina-
tion was unnecessary. It should be noted that in these
discrimination experiments (90, 91), arm and wrist
movements were studied, whereas for the precision
tasks described above (64, 65), finger movements were
necessary. The involvement of different muscle groups
in the two experimental situations may account for
the difference in conclusions. The experiments of
Laursen and Wiesendanger (91) and Laursen (90) are
important because they suggest that the pyramidal
tract participates in movements that involve learning
and selection.
In this section only representative studies that ex-
amined the permanent deficits produced by pyramidal
section were discussed. It should be noted, however,
that a well-known feature of the central nervous sys-
tem is "redundancy of function," and loss of function
produced by ablation of one system is rapidly compen-
sated for by other systems. Thus it is obvious that the
permanent functional deficits produced by pyramidal
section reveal only a part of pyramidal functions, all
of which cannot be explored by simply destroying the
pyramidal tract. However, whether the initial deficits
that recover as time passes are also due to the loss of
pyramidal function or to other factors such as pressure
temporarily produced by acute hemorrhage is difficult
to determine (37). This is one of the reasons why there

is still controversy between the interpretation of the
results of stimulation experiments and ablation exper-
iments.
SUMMARY
Twenty years have passed since the publication of
the chapter on the pyramidal tract by Patton and
Amassian in the Handbook of Physiology's first edi-
tion of the nervous system (123a). During this time a
remarkable progress has been made in our understand-
ings of the structure and function of this tract. De-
tailed distribution of the origin and the termination of
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CHAPTER 15: THE PYRAMIDAL TRACT 729
the pyramidal tract neurons has been worked out.
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