THE JOURNAL OF COMPARATIVE NEUROLOGY 228~105-116(1984)

Projections to the Frontal Cortex From

The Posterior Parietal Region in the
Rhesus Monkey
M. PETRIDES AND D. N. PANDYA
Department of Psychology and the Montreal Neurological Institute, McGill University,
Montreal, Canada H3A 2B4 (M.P.); and Edith Nourse Rogers Memorial Veterans
Hospital, Bedford, Massachusetts 01730, Departments of Anatomy and Neurology,
Boston University School of Medicine 02118, and Harvard Neurological Unit, Beth
Israel Hospital, Boston, Massachusetts 02215 (D.N.P.)

ABSTRACT
The projections to the frontal cortex from the various subdivisions of the
posterior parietal region in the rhesus monkey were studied by means of au-
toradiographic technique. The rostral superior parietal lobule (area PE) proj-
ects to the dorsal areas 4 and 6 on the lateral surface of the frontal lobe as well
as to the supplementary motor area (MII) on its medial surface. The caudal
area PE sends its connections to dorsal area 6 and MII. The projections from
the medial parietal cortex (areas PEc and PGm) are similar to those of the su-
perior parietal lobule but they tend to concentrate in the more rostral part of
dorsal area 6, MII, and in the cingulate gyrus (area 24). The most caudal part
of the medial parietal cortex also projects to area 8. The anteriormost part of
the inferior parietal lobule (area PF) projects to the ventral area 6, including
the caudal bank of the lower branch of the arcuate sulcus, to the ventral area
46 below the sulcus principalis, and to the frontal and pericentral opercular
cortex. The middle inferior parietal lobule (areas PFG and PG) projects to the
ventral part of area 46 and area 8, whilst the posteriormost inferior parietal
lobule (caudal PG and area Opt) is connected with both dorsal and ventral area
46, dorsal area 8, as well as the anteriormost dorsal area 6, and the cingulate
gyrus (area 24).

Key words: frontal, parietal, cerebral cortex, connections

It has previously been demonstrated that the posterior
parietal cortex is connected with the frontal cortex (Barbas
and Mesulam, '81; Chavis and Pandya, '76; Dekker et al.,
'75; Jacobson and Trojanowski, '77; Jones and Powell, '70;
Kuypers et al., '65; Pandya and Kuypers, '69). However, a
number of questions regarding these connections remain to
be answered. Previous studies had not investigated the
projections to the frontal lobe originating from the medial
part of the posterior parietal region and the cortex lying
within the intraparietal sulcus. For a complete view of
parietal lobe influences on the frontal lobe, it is essential
that these connections should also be studied. In addition,
the projections from the superior and inferior parietal lob-
ules, which have been demonstrated in earlier investiga-
tions, require further clarification, in particular with re-
gard to their field of termination and laminar distiribution
within the various cytoarchitectonic subdivisions of the
frontal cortex. Finally, with the exception of the earlier
studies of Krieg ('63) carried out with the Marchi technique,
no attempt has been made to describe the precise course of
the parietofrontal fibers. To address these issues, the parieto-
frontal connections in the rhesus monkey were reexamined
using the autoradiographic technique.
MATERIALS AND METHODS
Injections of radioactively labeled amino acids (3H-leucine
and/or -proline; volume range, 0.4-1.0 pl; specific activity
range, 40-80 pCi) were made in different parts of the pos-
terior parietal cortex in 19 rhesus monkeys. After a sur-
vival period of 3-7 days, the animals were killed and the
brains were processed for autoradiography (Cowan et al.,
'72). Exposure times ranged from 3 to 6 months. A series of
coronal sections of the hemispheres in which the injection
Accepted April 12, 1984.

0 1984 ALAN R. LISS, INC.

106
had been made were examined microscopically with dark-
field illumination. Labeled fiber bundles in the white mat-
ter and terminal labeling in the frontal cortex were traced
with the aid of an X-Y recorder that was electronically
coupled to the stage of the microscope. The injection and
termination sites, as well as the path of the labeled fibers,
were drawn on outlines of the surface of the brain using the
sulci as landmarks. The outlines of the surface of the cortex
were drawn from photographs of each brain taken before it
was sectioned. The thionin stain used in the preparation of
the histological material has allowed us to outline the cy-
toarchitectonic boundaries of the projection areas within
the frontal lobe.
RESULTS
In this report, the cytoarchitectonic areas of the posterior
parietal region are referred to in accordance with the par-
Fig. 1. Diagrams ot' the lateral, medial, and orbital surfaces of the cere-
bra1 hemisphere to shnw architectonic subdivisions of the frontal and par-
ietal lobes. The architectonic parcellation of the frontal lobe is according to
Walker ('40) and Barbas and Pandya ('82). The parietal-lohe parcellation is
according to Bonin and Bailey ('47) and Pandya and Seltzer ('82). Abhrevia-
tions in this and subsequent figures: AS, arcuate sulcus; CC, corpus cal-
losum; CF, calcarine tissure.: CING S, cingulate sulcus; CS, central sulcus;
M. PETRIDES AND D.N. PANDYA
cellation of Bonin and Bailey ('47) as well as that of Pandya
and Seltzer ('82). For the cytoarchitectonic subdivisions of
the frontal cortex, the nomenclature of Brodmann ('09) and
of Walker ('40) as modified by Barbas and Pandya ('82) is
used (Fig. 1).
Superior parietal lobule
In six cases (Fig. 2, cases 1-6) injections were made in dif-
ferent parts of the superior parietal lobule (areas PE and PEc)
including the adjacent upper bank of the intraparietal sul-
cus (area PEa). Figure 3 illustrates two cases: case 1with an
injection in the middle part of the upper bank of the intra-
parietal sulcus (area PEa) and adjacent superior parietal lob-
ule (area PE) and case 6 with an injection in the caudal part
of the superior parietal lobule (areas PE and PEc). The la-
beled fibers having emerged from the injection site de-
scended in the white matter between the medial parietal
G, gustatory area; IOS, inferior occipital sulcus; IPS, intraparietal sulcus;
LC, line of cut; LF, lateral (Sylvan) fissure; LS, lunate sulcus; OS, orbital
sulcus; OTS, occipitotemporal sulcus; POMS, parieto-occipital medial sul-
cus; F'S, principal sulcus; STS, superior temporal sulcus; RhF, rhinal fissure.
Designation Pro on the orbital and medial surfaces refers to proisocortices
with bilaminated appearance.
PARIETOFRONTAL CONNECTIONS 107

Fig. 2. Composite diagrams to show isotope injection sites on the lateral and medial surfaces of the parietal lobe.

cortex and the upper bank of the intraparietal sulcus and surface of the frontal lobe, terminal label was mainly seen
traveled rostrally to the frontal cortex maintaining a dorsal to be distributed in the lower bank of the cingulate sulcus
position between the cingulum bundle and the superior fron- and the adjoining cingulate gyrus, mostly within the caudal
tal gyrus. These fibers could be differentiated from those di- area 24. In addition, terminal label was observed in a more
rected toward the branstem, the corpus callosum, and the rostral location within the dorsal area 6 and in MI1 as
temporal lobe by their characteristic speckled appearance as compared with the location of label in these areas in the
a result of having been cut transversely in coronal sections. superior parietal lobule cases. There was also some label in
Most of the terminal label in each of these cases was seen at dorsal area 8 in the medial parietal cases. This was marked
the rostral border of area 4 and in the dorsal part of area 6 in case 9 with a more caudal extension of the injection site
lying above and in the caudal bank of the upper branch of the on the medial surface. Terminal label was distributed in a
arcuate sulcus. In case 1, label was also observed in area 4. columnar fashion throughout the entire thickness of the
There were also distinct clusters of terminal label in the up- cortex (Fig. 8D).
per bank of the cingulate sulcus and the adjacent cortex on
the medial part of the frontal lobe, a region correspondingto Rostal inferior parietal lobule
the supplementary motor area. A few fibers were observed to There were three cases with injections in the rostral part
terminate in dorsal area 46 and in ventral area 6. of the inferior parietal lobule, area PF (Fig. 2, cases 10-12).
The basic pattern of projections t o the frontral lobe was
similar in all three cases. As shown in Figure 5 (case lo),
Medial parietal cortex the labeled fibers traveled rostrally in the white matter of
In three cases (Fig. 2, cases 7-9), the injections were made the frontoparietal operculum. A large number of them ter-
in the cortex on the medial part of the parietal lobe involv- minated first in ventral area 6, in and around the lower
ing areas PEc and PGm as well as area PEci in the caudal limb of the arcuate sulcus. Other fibers continued rostrally
tip of the cingulate sulcus. The labeled fibers from these beyond the arcuate sulcus to terminate in the lower part of
cases traveled within the white matter in a manner similar area 46 lying below the sulcus principalis. In addition,
to that described for the cases of the superior parietal lob- terminal label was seen in two sites in the parietofrontal
ule. Many of these fibers, as illustrated in Figure 4, occu- operculum: in the pericentral part of the Sylvian opercu-
pied a position lateral to the depth of the cingulate sulcus lum, and in a more anterior location, in an area correspond-
and extended into the dorsal part of the cingulum bundle. ing to the “gustatory area” as described by Jones and
In the rostral part of their course, these fibers traveled Burton (‘76). In all these cases, terminal label was distrib-
through the white matter of the superior frontal gyrus. uted in all cortical layers in a columnar manner (Fig. 8E).
They terminated in the dorsal part of area 6, exhibiting a
tendency to concentrate in the more rostral parts of this Middle part of the inferior parietal lobule
region when compared with the termination pattern in this There were three cases (Fig. 2, cases 13-15) in which the
area of the superior parietal lobule cases. On the medial injection site occupied area PFG and the rostral part of area
108 M. PETRIDES AND D.N. PANDYA

4 5

q3
g,os- A S ’1 LF
LC

LC
1 2 3 4
W

STS

34 5 6 7

Fig. 3. Diagrammatic representations of isotope injection site of the surface of the hemishphere to show labeled fibers in white matter and
superior parietal lobule (shown in black) and distribution of resulting label terminal label in the cortex. The arcuate, principalis, lateral, cingulate, and
in the frontal lobe (shown as dots) in two cases. In this and subsequent intraparietal sulci are opened to expose both banks.
figures, the coronal sections are taken at the levels indicated on the lateral
PARIETOFRONTAL CONNECTIONS 109

L'C

CASE a
1

n
2 W
3 @

CASE 9

LC
n

6 7

Fig. 4. Diagrammatic representationof isotope injection sites on the medial surface of the parietal
lobe and the distribution of resulting label in the frontal lobe in two cases.
110
LC
4j6 i 6'9
CASE 10
Fig. 5. Diagrammatic representation of isotope injection in the rostral inferior parietal lobule and
the distribution of label in the frontal lobe in case 10. The lateral fissure is opened up to expose both
banks and the insula.
PG. In all three cases, the fibers originating from the injec-
tion sites and directed t o the frontal lobe entered the white
matter of the inferior parietal lobule and traveled rostrally
occupying a position just dorsal to the claustrum and the
circular sulcus of the insula. After having coursed under
the central sulcus and precentral gyrus, these fibers occu-
pied a position underneath the arcuate sulcus terminating
both in the premotor and prefrontal cortex. In case 13 (Fig.
6), in which the injection was in the dorsal part of PFG and
the intraparietal sulcus, terminal label was seen mainly in
area 8 and in area 46 in the lower bank of the sulcus
principalis. In case 15 (Fig. 61, in which the injection site
occupied the ventral part of area PFG and PG, terminal
label was mostly seen in the ventral and dorsal part of area
6, in dorsal area 8, and in area 46 in the sulcus principalis.
In this case, terminal label was also observed in the depths
of the cingulate sulcus and adjoining area 24 on the medial
surface of the frontal lobe. As in all previous cases, the
label was distributed in a columnar fashion throughout all
cortical layers.
Caudal inferior parietal lobule
Four cases had injections in the posteriormost part of the
inferior parietal lobule occupied by areas PG and Opt (Fig.
2, cases 16-19). As can be seen in Figure 7, the labeled
fibers directed toward the frontal lobe traveled rostrally in
the white matter between the intraparietal and lateral
sulci. Further forward, these fibers occupied a position above
the dorsal circular sulcus as well as medial to it. They
M. PETRIDES AND D.N. PANDYA
continued forward, passing first under the central sulcus
and then under the arcuate sulcus where they diverged in
several directions. Some fibers terminated in dorsal areas
6 and 8 in the upper limb of the arcuate sulcus, whilst
others continued forward to terminate in dorsal area 46
and area 9. Another component of these fibers occupied
area 46 in the lower bank of the sulcus principalis. In case
17, in which the isotope injected extended rostrally into the
lower bank of the intraparietal sulcus, an additional cluster
of label was observed in ventral area 46. In these cases,
labeled fibers were also seen in area 24 of the cingulate
gyrus and, as in all previous cases, the laminar distribution
of label was columnar in nature, extending through all
cortical layers (Fig. 8F).
DISCUSSION
The present investigation has shown that both the supe-
rior parietal lobule (rostral and caudal area PE) and the
medial part of the posterior parietal cortex (areas PEc and
PGm) project, primarily, to the dorsal part of area 6 and t o
a discrete part of the medial surface of the frontal lobe that
corresponds to the supplementary motor area. The projec-
tion to the dorsal area 6 originating from the superior
parietal lobule extends from the border of areas 4 and 6 t o
the caudal bank of the upper branch of the arcuate sulcus,
whilst the projection from the medial parietal cortex tends
to concentrate in the more rostral part of this area. In
addition, the more caudal part of the medial parietal cortex
PARIETOFRONTAL CONNECTIONS 111

LC

4 5 6/

CASE 13

LF
TS
TS

LC

CASE 15

LC

Fig. 6. Diagrammatic representation of isotope injections in the midinferior parietal lobule and
resulting label in the frontal lobe in two cases.
112 M. PETRIDES AND D.N. PANDYA

LC

CASE 16

LC

LC

CASE 17

LC

Fig. 7. Diagrammatic representation of isotope injections in the caudal portion of the inferior
parietal lobule and resulting label in the frontal lobe in two cases.
PARIETOFRONTAL CONNECTIONS 113

Fig. 8. Darkfield photomicrographs to show the location of labeled parietofrontal fibers in A (case
9). B (case lo), and C (case 16) and the distribution of the terminal label within the frontal lobe in D
(case (9), E (case lo), and F (case 16). ~ 6 . 5IPCD,
. inferior precentral dimple; SPCD, superior precentral
dimple.
114
projects to dorsal area 8 in the concavity of the arcuate
sulcus, and the cortex in the anterior parts of area PE and
upper bank of the intraparietal sulcus project to area 4.
These latter observations are consistent with those of Strick
and Kim ('78)and Jones et al. ('78). Whereas areas PE and
PEc project to the supplementary motor region on the me-
dial surface of the frontal lobe, area PGm favors area 24 of
the cingulate gyrus, and the rostral portion of the supple-
mentary motor area.
The projections to the frontal lobe from the inferior par-
ietal lobule (IPL) are somewhat more complex. The ante-
riormost part of the inferior parietal lobule (area PF)
projects to the ventral area 6 including the caudal bank of
the lower branch of the arcuate sulcus, to the ventral area
46 below the sulcus principalis, and to the cortex of the
rostral and pericentral frontal operculum. The middle infe-
rior parietal lobule (areas PFG and PG) projects to the
ventral part of area 46 as well as to area 8. The projections
to area 46 in the ventral bank of the sulcus principalis
appear to originate primarily from the more lateral parts
of this region, whilst those directed to the part of area 46
lying below the sulcus principalis and to area 8 seem to
originate from the more dorsal part of area PFG and PG
including the adjacent cortex lying in the lower bank of the
intraparietal sulcus (compare cases 12, 16, and 17). This
trend is in agreement with the previous observations of
Chavis and Pandya ('76). The most posterior part of the IPL
Fig. 9. Artist's schematic rendition of the trajectory of parieto-frontal fibers from the superior and
medial parietal lobe (I),the caudal inferior parietal lobule (111, and the rostral inferior parietal lobule
(111).For a description of these fiber bundles see text.
M. PETRIDES AND D.N. €'ANDYA4
(caudal area PG and area Opt) is connected not only with
ventral area 46 but also with dorsal area 46. In addition,
this region sends distinct projections to dorsal area 8 and to
the rostralmost portion of area 6 lying in the caudal bank
of the upper branch of the arcuate sulcus. Like area PGm
(medial parietal cortex), areas PG and Opt do not project
to the supplementary motor cortex on the medial surface
of the frontal lobe, but do project to the cingulate gyrus
(area 24).
The long association fibers joining the various areas of
the posterior parietal region to the frontal cortex are orga-
nized into distinct longitudinally running bundles. The fi-
bers emerging from the superior parietal lobule and the
medial posterior parietal cortex maintain a dorsal and me-
dial position in the medullary substance (Figs. 8A, 9). They
travel along the medial surface of the parietal and frontal
lobes dorsal to the cingulate gyrus. In contrast, the fibers
originating from the various parts of the inferior parietal
lobule occupy a more ventral and lateral position. Fibers
originating from the rostral part of the inferior parietal
lobule travel in the parietal and frontal opercula, whilst
those originating from the more caudal parts occupy a more
dorsal position coursing above the claustrum and the cir-
cular sulcus of the insula (Figs. 8B,C, 9). The classical
description of the superior longitudinal fasciculus referred
to a fiber system running dorsal to the claustrum and the
circular sulcus (Dejerine, 1895). This system was thought
 PARIETOFRONTAL CONNECTIONS 115
to connect temporal and parietal neocortex with the frontal and Opt) receive input from higher-order somatosensory
lobe. The present investigation has shown that the poste- areas (PFG and PGm), polymodal areas in the superior
rior parietal region is connected with the frontal lobe by temporal sulcus, and the cingulate and parahippocampal
means of three relatively distinct fiber systems originating gyri (Mesulam et al., '77; Pandya and Seltzer, '82; Stanton
from the medial parietal region and the superior parietal et al., '77). Area Opt receives, in addition, direct input from
lobule, the rostral parts of the inferior parietal lobule, and the visually related area OA (Pandya and Seltzer, '82). The
the more caudal parts of the inferior parietal lobule. cells of the caudal inferior parietal lobule exhibit properties
There is considerable evidence from investigations of the that differ from those of the more rostral part in that they
behavioral deficits resulting from damage to the frontal appear to be more closely related to the visual modality
cortex in man and other animals that this part of the cortex (Hyvarinen and Shelepin, '79; Mountcastle et al., '75; Ro-
subserves complex regulatory processes (Fuster, '80; Luria, binson et al., '78). The caudal inferior parietal lobule pro-
'66; Milner, '82). For example, impairments have been dem- jects extensively to area 46 within the prefrontal cortex.
onstrated after frontal lobe lesions in man and monkey on Lesions of area 46 in the monkey and in particular that
tasks that require changes of response patterns (e.g., Iver- part of it lying in the sulcus principalis have been shown to
sen and Mishkin, '70; Milner, '64; Mishkin, '64) as well as cause impairments on various complex tasks such as spa-
on tasks that require the organization of a sequence of tial delayed alternation and delayed response (e.g., Butters
responses (Brody and Pribram, '78; Petrides and Milner, et al., '71; Gross and Weiskrantz, '62; Mishkin, '57).
'82; Pinto-Hamuy and Linck, '65). The frontal cortex is a
large area that is heterogeneous both in terms of structure
and function. It receives input from a variety of cortical ACKNOWLEDGMENTS
association areas, some of which provide modality specific This work was supported by E.N.R.M. Veterans Hospital,
input and others multimodal input (Barbas and Mesulam, Bedford, MA, NIH grant NS26841 to D.N. Pandya, and
'81; Chavis and Pandya, '76; Jones and Powell, '70). The NSERC grant A7466 to M. Petrides. We are thankful to
present work has shown that the posterior parietal region Mr. Brian Butler and Ms. Lydia Kenton for excellent tech-
(including the medial posteior parietal area) projects to a nical assistance.
restricted part of the dorsolateral frontal cortex (areas 6, 8,
9, and 46) and to the supplementary motor cortex. Within
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