254 T I N S - J u n e 1986

The relatlo hlp of perceived pain conduct impulses into the region of the
recording tip. This suspected presence
to afferent nerve impulses of temporary partial block does not cast
doubt in any way on the validity of the
The word nociceptor is a purely properties of the receptive field of the recordings from those fibres that are
physiological term meaning a nerve fibre. As one group recently concluded, conducting.
fibre that responds to stimuli that 'These findings endorse the concept A sensation can be described in terms
damage tissue or would damage tissue if that the quality of sensation is coded in of threshold, intensity, time course and
they were prolonged. The word pain is a specific sensory systems. Further, they location, and the firing of afferent units
purely psychological term defined as 'an provide novel evidence that sensory can be assessed for correlates of these
unpleasant sensory and emotional quality, magnitude and localization can aspects of sensation. The fibres of
experience associated with actual or be exquisitely resolved at cognitive particular interest are obviously those
potential tissue damage or described in levels on the basis of input initiated in a with high thresholds, such as those in the
terms of such damage'. What then is the single mechanoreceptor unit '9. We A delta group of small myelinated fibres
relation between the physiological have challenged these interpretations and in the C group of unmyelinated
existence of impulses in nociceptors and on a number of technical grounds; they fibres 11-13'~5. It might be expected that
the psychological response? For visceral are discussed fully elsewhere 1°. the onset of firing of one of these types of
pain, the question may not even arise, Here we wish only to point out that fibre would invariably coincide with the
since the existence of specific visceral there are objections to these con- onset of pain, but this has not been
nociceptors is strongly doubted. But clusions and to correct any impression observed. Both groups of fibres begin to
nonetheless, most textbooks of phy- that the work supports the notion that respond to pressure or chemicals or heat
siology and neurology imply that pain is pain is the equivalent of afferent at stimulus intensities well below those
a unique consequence of impulses in nociceptor discharge. In fact, even the that evoke pain. To take C fibres
nociceptors by referring to pain fibres, microneuronographers themselves do responding to heat as an example, most
pain cells and pain tracts. For instance, a not make the same claims for pain as fibres begin responding at 41°C while
recent text specializing in neuroscience they do for touch, although it is easy to the pain threshold can be as high as
states 'primary pain afferents terminate see how their general conclusions 49°C. In this study, the authors conclude
in the dorsal horn of the spinal cord', regarding cutaneous sensibility might that central spatial summation from
and 'the pain projection pathways are be taken to apply to pain. many nociceptors is necessary before
collectively called the anterolateral Hagbarth and Vallbo inserted tung- pain is sensed 16. Another group show
system '1 . sten microelectrodes by hand per- that 'subjective ratings give a better
The recent developments that have cutaneously into human peripheral estimation of stimulus size than did the
greatly advanced this field began in 1968 nerves and recorded from single discharge rates of the individual (
when Hagbarth and Vallbo 2'3 showed myelinated fibres. By 1970, Torebj6rk fibres'~5. It is apparent that the ability to
that it was possible to record the and Hallin were recording from single establish a threshold and to estimate
activity of single afferent nerve fibres in unmyelinated fibres ll'12, soon followed intensity is not determined by the
human peripheral nerves, and thus by the Belgian team of Van Hees and properties of single peripheral fibres or
directly compare sensation with prim- Gybels 13. Since then many papers have even types of peripheral fibre. Rather
ary afferent discharge patterns. For been published from Sweden and the periphery feeds information that is
cutaneous sensations, the results do not Belgium on impulses in motor, sym- then interpreted in terms of threshold
support the classical view, which is still pathetic and sensory axons. The and intensity by central structures.
adopted by so many. Rather they recordings fulfil all the classical criteria An example of such central analysis is
demonstrate that the threshold, inten- of single units in their shape, velocity, seen when pain is evoked by either a hot
sity, quality, time course and location of threshold and all-or-none characteris- punctate stimulus or by punctate
perceived pain is determined by central tics. Furthermore the stimulus-res- pressure. The subject cannot differen-
mechanisms that take into account ponse properties fall into the same tiate between the two stimuli. The C
several specifiable factors in addition to groupings with respect to stimulus fibre firing rate when the stimulus
the firing of nociceptors. This article type, threshold and adaptation as have becomes painful is 0.5 Hz for the heat
will consider these factors in some been recorded in single animal axons stimulus and over 10 Hz for the pressure
detail. isolated by dissection. This ability to stimulus. This difference is predicted by
In the last few years the microneuron- record single units is particularly the gate control theory and is explained
ographers have introduced a new surprising when the relative size of the by the fact that the pressure stimulus
technique in which they pass current exposed microelectrode tip is compared activates both high and low threshold
through their recording electrodes and to the size of the axons (see Fig. 1 in Ref. mechanoreceptors. The low threshold
claim to stimulate the same fibre that 14). Some groups have also used either mechanoreceptors mostly connected to
they had been recording from, and that smaller or larger tips with similar large myelinated afferents exert an
fibre only4-8. The approach has been results. The most likely explanation of inhibitory effect on the central excita-
applied to a range of tactile cutaneous these single unit recordings is that the tion produced by small afferents ~7. It is
afferents, and the general conclusion of presence of the electrode and its therefore necessary to generate a larger
these workers is that activation of a manipulation induces a pressure block afferent barrage in small fibres to
single afferent nerve fibre gives rise to a of the majority of the nearby fibres produce the same central effect if there
sensation that corresponds to the allowing only one or a few axons to is concurrent activity in large fibres.
© 1986, E l s e v i e r S c i e n c e P u b l i s h e r s B . V , A m s t e r d a m (1378 - q 9 1 2 / 8 6 / $ 0 2 II~l
TINS-June 1986
This is an example of the CNS
responding in a context that takes into
account a combination of different
types of afferent input.
Different groupings of afferents may
generate identical pain sensations. For
example, subjects cannot differentiate
between painful punctate hot, cold or
pressure stimuli. On the other hand, the
same stimulus can generate different
sensations depending on its area. At
43°C a 1 mm diameter probe produces
prickingpain, a2-5 mmdiameterprobe
stinging pain, and a 20 mm diameter
probe pleasant warmth 17. This evidence
shows that the CNS is analysing
modality and intensity not only on the
basis of firing frequency in particular
afferents but also by taking into account
the spatial gradient of the stimulus. This
contradicts the classical view that
modality is determined by the activation
of modality-labelled specific fibres that
end in local skin spots. Spot-like
variations in sensitivity exist but they
cannot be attributed to the local
presence of special nerve fibres for the
following reasons. The spots rapidly
move, appear and coalesce. They are
not associated with particular types of
ending. There are far more endings than
spots. The size of the spot depends on
the size of the stimulus17-2°.These facts
require that the central processing of the
afferent barrage take into account
which groups of fibres are responding,
what is their relative frequency of
discharge, and what is the spatial
gradient of responding fibres.
The conclusion that central processes
determine threshold, intensity and
modality is even more apparent when
the time course of sensation is compared
with the time course of the afferent
barrage. For 15 s painful heat or
pinch stimuli, A delta fibres fire in a
rapid high-frequency burst lasting
about 5 s and then become silent or fire
at a very low frequency. As the rate of
firing decreases, the subject begins to
report pain (the mismatch in time is not
attributable to peripheral delays). A
similar mismatch of onset is reported for
C fibres. The pain continues to increase
after the fibres decrease their firing,
even for seconds after firing has ceased.
255
It is evident that the time course of properties of nociceptors. The response
sensation is determined by central of nociceptors is one of the factors
factors other than the arrival of the incorporated into the central analytic
afferent barrage 21. mechanisms that can generate many
The results discussed so far come perceptual syndromes including pain.
from normal volunteers who are trained
and attentive and subject to brief P. D. WALL AND S. B. McMAHONt
harmless stimuli. If even they cannot Cerebral Functions Research Group, Department
sense the painfulness of a stimulus as of Anatomy, University College London, and
encoded in a special set of afferents, it is t Department of Physiology, St Thomas's Hospital
Medical School, London SE1, UK.
not surprising that the slings and arrows
of the real world produce pain by
Selected references
mechanisms that require more factors
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