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Parallel Processing of Cutaneous Information in the Somatosensory System of the Cat

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Parallel Processing of Cutaneous Information in the Somatosensory System of the Cat LE JOURNAL CANADIEN DES SCIENCES NEUROLOGIQUES Parallel Processing of Cutaneous Information in the Somatosensory System of the Cat ROBERT W. DYKES RESUME: Dans le passe le principe de In the past, studies of the somatosen­ beginning (Adrian, 1941) although it base des mecanismes corticaux du systeme sory system have played a major role was not reported in man until much sensitif furent fondes en grande partie sur in developing ideas central to under­ later (Penfield and Rasmussen, 1950). le resultat de Vetude du systeme somato- standing cortical mechanisms ap­ Woolsey and Fairman (1946) found sensitif. Les idees de cartes topographiquesplicabl e to all sensory systems. The SII in a number of primates and sub- de colonnes corticales, de specificite ideas of (i) topographic maps, (ii) cor­ primates and hypothesized that the se­ module, ont toutes originees dans Vetude detica l columns, and (iii) modality cond somatosensory map was an ce systeme, pour etre ensuite appliquees aux systemes auditifs et visuels. Re'cem- specificity originated in this sensory evolutionarily more primitive projec­ ment des changements fondamentaux se system and were later applied to the tion of the body surface that had been sont produits dans notre comprehension auditory and visual systems. Now, superceded by a newer projection to SI. des fonctions somatosensitives et corticales, after several decades of relative con­ These classical experiments il­ ces concepts nouveaux s'appliqueront bien-stancy, our ideas about somatosensory lustrated the regularity of the represen­ tdt aux autres systemes. Le present article cortical function have begun to change tation of the body surface on the cor­ detaille ces developpements. rather rapidly and again the newer tical surface. With the exception of the ideas may find useful applications in hand-face transition, the representation other sensory systems. In this article appeared to follow a sequence dictated the concepts found in current textbooks by the dermatomal sequence of spinal are summarized briefly and the many nerves (Bard, 1938). The maps were elegant experiments which expanded shown to be distorted in a character­ and filled out the details of these istic manner so that the body parts with traditional ideas are noted only briefly the greatest innervation density were so that there is space to present some given a much larger proportion of the of the newer ideas about the somato­ cortical surface. In fact, the size of a sensory system. cortical area devoted to a particular body part is thought to be propor­ tional to, and dictated by, the innerva­ THE TRADITIONAL VIEWS tion density of that part (Mountcastle, Somatosensory Maps: The Homun- 1980). culus A map of the body surface spread on the postcentral gyrus was The Cortical Column and Modality published by Penfield and Boldrey in Specificity In 1957, Mountcastle 1937 (Fig. 1) and eventually became recorded from 685 single units in areas known as the homunculus. Woolsey 3a, 3b, 1, and 2 of cat somatosensory and his colleagues mapped many cortex. When electrodes were inserted species in the next 25 years and drew perpendicular to the surface, all corresponding animal shapes over the neurons encountered were of one postcentral gyrus or its homologue in modality and had overlapping receptive each species studied (Woolsey, 1958; fields. When vertically-oriented 1964). No one questioned the validity electrode penetrations were not exactly of this conceptualization. Instead, dis­ perpendicular to the cortex, abrupt cussions focussed on the details of the shifts in the nature of the adequate organization of the maps. For example, stimulus were observed. As the the relationships between the orienta­ electrode advanced, regions driven by tion of the occiput, hand, and face were cutaneous stimuli gave way to regions From the Microsurgical Research Laboratories. Departments of Neurology and Neurosurgery, discussed in great length (Woolsey, driven by stimulation of deep structures Physiology and Surgery. Royal Victoria Hospital, 1958; Penfield and Jasper, 1954). or conversely responses driven by deep McGill University, Montreal, Quebec. The existence of a second somato­ stimulation changed to responses best Reprint Requests to: Dr. R.W. Dykes, driven by cutaneous stimuli during the Microsurgical Laboratories, Royal Victoria Hospital, sensory representation in the cerebral McGiU University, Montreal, Quebec. cortex (SII) was apparent from the electrode trajectory. From this data he Vol. 9 No. 1 FEBRUARY 1982—9 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.22, on 25 Sep 2021 at 14:00:48, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0317167100043560 THE CANADIAN JOURNAL OF NEUROLOGICAL SCIENCES Levitt, 1968; Dreyer et al, 1975) con­ firming the existence of functionally homogenous regions separated by boundaries where the function and receptive field change abruptly. Com­ parable functional units were reported in the visual cortex (Hubel and Wiesel, 1962) soon after their description in the somatosensory cortex and equivalent, vertically-arranged functional units were reported in the auditory cortex (Hindetal., 1960). Modality Specificity of Cortical Neurons Included in the columnar hypothesis, although not stated ex­ plicitly, was the principle of modality specificity: That is, despite the multiple opportunities for the convergence of several classes of sensory receptors onto one cortical neuron, the neurons within one vertically-oriented region of primary somatosensory cortex, when activated by natural stimuli, appeared to receive excitatory inputs from only one class of receptors while adjacent areas were best activated by other clas­ ses. The modality classification employed by Mountcastle (1957) in­ cluded hair, pressure, deep, and joint responses. Several examples of modality-specific neurons for each of these classes were presented in the ear­ ly publications from his laboratory but no evidence of neurons activated by more than one class. (Mountcastle, 1957; Powell and Mountcastle, 1959; Mountcastle and Powell, 1959.) Neurons activated principally by one class of afferent input have now been reported at each level of the neuraxis, including submodality-specific neurons activated by cutaneous slowly adapting receptors, cutaneous rapidly adapting receptors, muscle spindle afferents, joint afferents and afferent fibers from pacinian corpuscles (Dykes, 1978). Neurons activated specifically by nox­ ious stimuli, warm stimuli and cold Figure 1 — (Reproduced with permission from Penfield and Boldrey, 1937) The single map of the stimuli have been identified in the body surface called the homunculus extending over the entire primary somatosensory cortex. The map is bilateral because one side is meant to represent the motor cortex and the other the spinal cord and thalamus (cf Willis and sensory cortex. Coggeshall, 1978). So far the cortical projection of modality specific neurons of these latter classes has eluded the formulated an hypothesis stating that the regions of SI caudal to area 3 while microelectrode. the somatosensory cortex contained a the proportion of cutaneous responses mosaic of functional units consisting of were greatest in the center of the These three concepts; the maps, the vertical columns of neurons serving (i) somatosensory cortex. Subsequent to columns, and the modality specificity one point on the body and (ii) one class these experiments, cortical columns of somesthetic neurons are major parts of sensory receptors. The proportion of have been studied by numerous of the foundation upon which our un­ deep columns were said to be greater in workers (Welt et al, 1967; Levitt and derstanding of the functioning of the Downloaded10 —FEBRUAR from https://www.cambridge.org/coreY 1982 . IP address: 170.106.33.22, on 25 Sep 2021 at 14:00:48, subject to the Cambridge Core terms of use, availableSomatosensory at Processing https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0317167100043560 LE JOURNAL CANADIEN DES SCIENCES NEUROLOGIQUES TABLE 1 Peripheral afferent nerve fibers in primates and their roles in sensation* Type Fiber class, size, and Peripheral Differential sensitivity of skin conduction velocity termination and adaptive propertyt Sensory function Glabrous A-beta,* 6-12/x, Merkel's cells SA mechanoreceptors Velocity and position detectors; 35-75 ni/sec sense of touch-pressure Meissner's cor- QA mechanoreceptors Velocity and perhaps instanta­ puscles neous position; sense of con­ tact and flutter; best at 30-40 Hz Pacinian corpuscles QA mechanoreceptors Velocity and perhaps higher de­ rivatives of position; sense of contact and vibration: best at 250-300 Hz A-delta, 1-5/z, 5-30 Bare nerve endings SA thermoreceptors Sense of cooling m/sec Bare nerve endings SA nociceptors Sense of pricking pain and, at low frequencies, tickle C fibers, 0.2-1.5 zi, Bare nerve endings SA thermoreceptors Sense of warming 0.5-2 m/sec Bare nerve endings SA nociceptors Sense of burning pain and, at low frequencies, itch Hairy A-bcta,* 6-12 ti, Hair follicle ap­ QA mechanoreceptor Velocity detectors; sense of con­ 35-75 m/sec paratus tact and flutter; best at 30-40 Hz Bare nerve endings, QA mechanoreceptor Velocity detectors; sense of con­ "field" recep­ tact tors Pinkus domes, SA "type I" mech­ Stimulation in human elicits Merkel cells anoreceptor no sensation Ruffini organs SA "type II" mech­ Velocity and position detectors; anoreceptor sense of touch-pressure Pacinian cor­ QA mechanoreceptor Velocity and perhaps higher de­ puscles rivatives of position; sense of vibration; best at 250-300 Hz A-delta, 1-5 p., Bare nerve endings QA mechanoreceptor Velocity; sense of contact 5-30 m/sec Bare nerve endings SA thermoreceptor Sense of cooling Bare nerve endings SA nociceptors Sense of pricking pain and, at low frequencies, tickle C fibers, 0.2-1.5 tt, Bare nerve endings SA thermoreceptors Sense of warming 0.5-2 m/sec Bare nerve endings SA nociceptors Sense of burning pain and, at low frequencies, itch Bare nerve endings SA mechanoreceptors Occur rarely in monkey skin and not present in human skin *In earlier classifications these fibers were labeled A-alpha.
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