JOURNALOF NEUROPHYSIOLOGY Vol. 66, No. 3, September I99 1. Printed in U.S.A.
Reorganization of Somatosensory Area 3b Representations in Adult Owl Monkeys After Digital Syndactyly T. ALLARD, S. A. CLARK, W. M. JENKINS, AND M. M. MERZENICH Departments of Otolaryngology and Physiology, University of California at San Francisco Medical Center, San Francisco, California 94143
SUMMARY
AND
CONCLUSIONS
1. These experiments were designed to test the hypothesis that temporally correlated afferent input activity plays a lifelong role in the establishment and modification of receptive fields (RFs) and representational topographies in the primary somatosensory cortex of adult monkeys. They were based in part on the finding that adjacent digits of the hand are represented discontinuously in area 3b of the adult owl monkey. If cortical receptive fields and the details of cortical topographic representations are shaped by the weights of the temporal correlations among afferent inputs, then representational discontinuities between digits would be expected to arise because inputs from the skin surfacesof adjacent digits are largely independent in the critical time domain. 2. In the present experiments, the skin of adjacent digits 3 and 4 of the monkey hand was surgically connected to create an artificial syndactyly, or webbed-finger condition. Highly detailed microelectrode maps of the cortical representation of the syndactyl digits were obtained 3-7.5 mo later. This experimental manipulation greatly increased the amount of simultaneous or nearly simultaneous input from the normally separated, now fused, surfaces of adjacent fingers. 3. Cortical maps of the representations of finger surfaces were highly modified from the normal after a several-month-long period of digital fusion. Specifically, the normal discontinuity between the cortical representations of adjacent fingers was abolished. Within a wide cortical zone, RFs were defined that extended acrossthe line of syndactyly onto the surgically joined skin of both fused digits. The representational topography of the fused digits was similar to any normal single digit and was characterized by a continuous progression of partially overlapping RFs. 4. Control observations revealed that these reorganizational changes cannot be accounted for by any changes in cutaneous innervation induced by the surgery. They must arise from representational changes in the central somatosensory system. 5. These findings reveal that cortical maps can be altered in detail in adult monkeys by modifying the distributed temporal structure of afferent inputs. They support the longstanding hypothesis that the temporal coincidence of inputs plays a role in the grouping of input subsets into specific cortical RFs and, consequently, in the shaping of selected effective cortical inputs and representational topographies throughout life. INTRODUCTION
Recent electrophysiological experiments conducted within primary somatosensory cortical (SI) fields in adult rats, cats, raccoons, and monkeys have shown that the topographic cortical representations of the skin surfaces within these zones can be substantially altered after peripheral denervation (Dykes and Lamour 1988; Franck 1980; Kalaska 1048
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and Pomeranz 1979; Kelehan and Doetsch 1984; Merzenich et al. 1983a,b, 1984b; Rasmusson 1982; Wall and Cusick 1984, 1986), after differential use of limited skin surfaces in a behavioral task (Jenkins et al. 1990; Merzenich et al. 1988), or after restricted cortical lesions (Jenkins and Merzenich 1987; Pons et al. 1988). Throughout the lifespan of an adult mammal, somatosensory receptive fields (RFs) for neurons at specific cortical sites can enlarge or contract, and the cutaneous locations of their RFs can shift relatively long distances over the skin (see Merzenich 1985, 1987; Merzenich et al. 1984a, 1988 for review). Throughout these different reorganizational sequelae, a basic plan of local topography is usually conserved that is characterized by partially overlapping RFs defined at neighboring loci across the cortical surface (Jenkins and Merzenich 1987; Jenkins et al. 1990; Merzenich et al. 1983a,b, 1984b). We have previously argued that this dynamic representational remodeling might be accounted for by changes in the effectiveness of existing cortical synapses (Merzenich 198 5, 1987; Merzenich et al. 1984a, 1988). Thus reconstructed thalamic arbors extend beyond physiologically identified target zones in the more refined cortical map (Garraghty and Sur 1990; Kosar and Hand 198 1; Landry and Deschenes 198 1; Snow et al. 1988), cortical RFs rapidly enlarge severalfold in extent after topical administration of bicuculline (Dykes et al. 1984; Hicks and Dykes 1983) or after peripheral nerve stimulation (Recanzone et al. 1990), and excitatory postsynaptic potentials can be evoked in cortical neurons from skin sources far beyond those that effectively drive them under natural stimulation (Macgillis et al. 1983; Zarzecki et al. 1983; Zarzecki and Wiggin 1982). These and other data indicate that the specific subset of inputs comprising a cortical RF at a specific time in the life of an adult mammal is dynamically selected from a far larger array of anatomically existing inputs (Edelman 198 1; Edelman and Finkel 1984; Merzenich 1985, 1987; Merzenich et al. 1984a, 1988). Neurons at any given cortical location can be driven by many different combinations of inputs, comprising hundreds to thousands of different RFs at different times in a lifetime. Given this marked lifelong representational dynamism, what mechanisms underlie the process by which specific inputs are grouped into cortical RFs at any given time? What is the basis for the partially shifted RF overlap at neighboring cortical loci that is characteristic of topography in area 3b of SI? We have earlier hypothesized that this process of input selection is based on the temporal synchro-
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nization of inputs and on a system of horizontal network influences by which inputs at any given location influence inputs selected by their neighbors (Merzenich 1985, 1987; Merzenich et al. 1984a). The present experiments are designed to provide a simple test of this hypothesis. In normal adult owl monkeys, individual digits are represented in a segregated fashion in cortical area 3b. The skin of adjacent digits is represented in discrete cortical zones with abrupt borders, differentiating one digit’s representation from its neighboring digit’s representation. On either side of these representational discontinuities, neurons usually are driven exclusively by stimulation of one or the other of the two bordering digits. That is, RFs are almost always restricted to single digits. According to our hypothesis, the cortical representations of individual adjacent digits are not segregated by their anatomic connections, but because the activity of peripheral inputs from the independent skin surfaces of adjacent fingers is relatively poorly correlated in the critical time domain (tens of milliseconds). In support of this claim, we have already demonstrated that anatomic inputs from single thalamic neurons in the cat commonly project across the lines of representational discontinuities in the cortex (Snow et al. 1988) and that, in many representational remodeling experiments in monkeys, discontinuities between the representation of digits appear to move long distances across the cortex (Jenkins and Merzenich 1987; Merzenich et al. 1983a,b) and to reform between newly apposed digits after amputation (Merzenith et al. 1984b). These studies strongly indicate that the recorded representational discontinuities in cortical maps are functional, and not anatomic, entities. If that is the case, and if input selection and topographies are based on the temporal coincidence of afferent inputs, then discontinuities in representation between digits in monkeys should be abolished by increasing the temporal coactivation of inputs from adjacent fingers, thereby creating a large pool of potential RFs combining inputs from both digits. Increased coactivation of inputs from adjacent fingers can be achieved by mechanically coupling the skin surfaces of those digits surgically, thereby creating an artificial syndactyly, or webbed-finger condition. This fusion of the skin of the two digits should result in temporally synchronous stimulation across the newly adjoined skin, much like that normally occurring across a single digit. In these studies, consistent with our hypothesis, fusion of two adjacent digits resulted in a disappearance of the normal discontinuity between digit representations and the emergence of a broad region of cortex with single-component RFs combining inputs from both syndactyl digits. Preliminary reports of these results have been published earlier (Allard et al. 1985; Clark et al. 1988). METHODS
The dorsal and volar skin of digits 3 and 4 of the hands of adult owl monkeys (Aotus nancymai) were surgically connected from distal to proximal phalanges, creating syndactyl fingers in three intensively studied cases.After 14, 25, or 33 wk, a single, highly detailed map of the cutaneous representation of these digits and adjacent skin surfaces was obtained in the primary koniocortical SI field, area 3b, in each case.Similarly detailed cortical maps have
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also been derived in a series of normal (control) monkeys (Merzenith et al. 1987; Stryker et al. 1987). Peripheral hand surgeries All initial hand surgeries were conducted under sterile conditions and with the use of conventional human surgical procedures by an experienced surgeon with expertise in human plastic surgery and microsurgery (S. A. Clark). General anesthesia was induced and maintained by the use of halothane (l-2%) in a nitrous oxide (1.5 l/min)-oxygen (0.5 l/min) mixture. Core body temperature was monitored and maintained at 375°C with a feedback-controlled heating pad. The arm was exsanguinated with a tourniquet following conventional human protocols. Incisions were made with the aid of a surgical microscope along the midlateral lines of ulnar digit 3 and radial digit 4. This line sharply demarcates the limits of distribution of the digital cutaneous nerves innervating volar glabrous and dorsal hairy digital skin. Dorsal and volar skin flaps were sewn together along their entire lengths with 8-O vycril suture on a microsurgical needle to minimize tissue trauma. Total tourniquet time was 2 mm in cats and monkeys (Garraghty and Sur 1990; Kosar and Hand 198 1; Landry and Deschenes 198 1; Snow et al. 1988), and inputs from even more distant peripheral sources can evoke excitatory postsynaptic potentials in cortical neurons (Macgillis et al. 1983; Zarzecki et al. 1983; Zarzecki and Wiggin 1982). On the other hand, it is not clear why normal distance limits are exceeded in these fused-digit cases or why persistent patches representing skin along the scar line can be found throughout the zone of representation of digits 3 and 4. In a normal map of a sinDORSAL DIGIT REPRESENTATION. gle digit, the representation of the glabrous skin is often a contiguous uninterrupted patch that is bordered in some places by the representation of hairy skin. In the present series, the fused glabrous representation of digits 3 and 4 was partially interrupted in each case by a large central patch of hairy skin representation. This segregated patch of dorsal representation on the middle and proximal phalanges was completely surrounded by glabrous RFs representing the skin of the fused digits. This central patch of hairy skin representation may have existed in the same position before the surgical syndactyly. If this were the case, the dorsal patch would serve as a marker of the original abrupt discontinuity between digits 3 and 4 that must have existed before the syndactyly surgery was performed. Under these circumstances, the emergence of universally double-digit dorsal fields would merely reflect the changing temporal structure of their original driving inputs. Alternatively, other factors associated with the syndactyly itself could induce the formation of a dorsal patch of double-digit RFs at a point in the cortical zone intermediate between the normal representation of digits 3 and 4. Some inputs from the radial nerve supplying the dorsum of the hand are actively suppressed in the central representation of the glabrous hand (Merzenich et al. 1983a,b); median nerve section produces an immediate unmasking of hairy inputs to the hand region in area 3b of adult owl monkeys. It is possible that a dorsal representation could emerge within a formerly glabrous region, exploiting existing but suppressed inputs from the hairy skin. NONCONTIGUOUS RFs. Noncontiguous double-digit RFs occurred at the distal tips of digits 3 and 4. These dual-component RFs almost certainly reflect the consequences of central reorganization, rather than abnormal peripheral innervation (see above). Noncontiguous fields were not found in a segregated topographic region, but they did respect the general plan of proximal-to-distal organization in the syndactyly zone. It appears likely that the temporal synchronization of afferent inputs is a principal factor that determines which input combinations contribute to RFs. The emergence of these noncontiguous RFs provides evidence that there is no a priori requirement that afferent inputs selected to gener-
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ate given RFs be continuous. If this is the case, then why are neighboring RFs normally continuous, as a rule? We hypothesize that normal RF structure simply manifests the fact that incident stimulation of the skin results in costimulation at distant or separated skin locations with low probability. By contrast, immediately adjacent neighboring skin locations that are mechanically coupled have a relatively higher probability of coincident or correlated stimulation. This hypothesis is subject to simple experimental testing now being initiated in our laboratory. We thank G. Recanzone and R. Nudo for important technical advice and assistance. This research was supported by National Institute of Neurological Disorders and Stroke Grant NS- 104 14, the John C. and Edward Coleman Memorial Fund, and Hearing Research. Address for reprint requests: T. Allard, Cognitive and Neural Sciences (1142), Office of Naval Research, 800 N. Quincy St., Arlington, VA 222 175000. Received 26 July 1988; accepted in final form 25 April 199 1. REFERENCES T. Biological constraints on a dynamic network: the somatosensory system. In: Connectionist Modeling and Brain Function: The Developing Interface, edited by S. J. Hanson and C. Olson. Cambridge, MA: MIT Press, 1990, p. 132- 163. ALLARD, T., CLARK, S. A., JENKINS, W. M., AND MEFUENICH, M. M. Syndactyly results in the emergence of double-digit receptive fields in somatosensory cortex in adult owl monkeys. Sot. Neurosci. Abstr. 11: 965, 1985. ALLOWAY, K. D., SINCLAIR, R. J., AND BURTON, H. Responses of neurons in somatosensory cortical area II of cats to high frequency vibratory stimulation during iontophoresis of a GABA antagonist and glutamate. Somatosens. Mot. Res. 6: 109- 140, 1988. CALFORD, M. B. AND TWEEDALE, R. Immediate and chronic changes in responses of somatosensory cortex in adult flying-fox after digit amputation. Nature Lond. 332: 446-448, 1988. CLARK, S. A., ALLARD, T., JENKINS, W. M., AND MERZENICH, M. M. Receptive fields in the body-surface map in adult cortex defined by temporally correlated inputs. Nature Lond. 332: 444-445, 1988. DYKES, R. W. AND LAMOUR, Y. An electrophysiological laminar analysis of single somatosensory neurons in partially deafferented rat hindlimb granular cortex subsequent to transection of the sciatic nerve. Brain Res. 449: 1-17, 1988. DYKES, R. W., LANDRY, P., METHERATE, R., AND HICKS, T. P. Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons. J. Neurophysiol. 52: 1066- 1093, 1984. EDELMAN, G. M. Group selection as the basis for higher brain function. In: Organization of the Cerebral Cortex, edited by F. 0. Schmitt, F. G. Worden, G. Adelman, and S. G. Dennis. Cambridge, MA: MIT Press, 1981, p. 51-100. EDELMAN, G. M. AND FINKEL, L. H. Neuronal group selection in the cerebral cortex. In: Dynamic Aspects of Neocortical Function, edited by G. M. Edelman, W. E. Gall, and W. M. Cowan. New York: Wiley, 1984, p. 653-695. FRANCK, J. I. Functional reorganization of cat somatic sensory-motor cortex (SmI) after selective dorsal root rhizotomies. Brain Res. 186: 458462, 1980. GARDNER, E. P. Somatosensory cortical mechanisms of feature detection in tactile and kinesthetic discrimination. Can. J. Physiol. Pharmacol. 66: 439-454, 1988. GARRAGHTY, P. E., PONS, T. P., SUR, M., AND KAAS, J. H. The arbors of axon terminations in middle cortical layers of somatosensory area 3b in owl monkeys. Somatosens. Mot. Res. 6: 40 l-4 11, 1989. GARRAGHTY, P. E. AND SUR, M. Morphology of single intracellularly stained axons terminating in area 3b of macaque monkeys. J. Comp. Neural. 294: 583-593, 1990. HEBB, D. 0. The Organization of Behavior. New York: Wiley, 1949. ALLARD,
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T. P. AND DYKES, R. P. Receptive field size for certain neurons in primary somatosensory cortex is determined by GABA-mediated intracortical inhibition. Brain Res. 274: 160- 164, 1983. IWAMURA, Y., TANAKA, M., SAKAMOTO, M., AND HIKOSAKA, 0. Functional subdivisions representing different finger regions in area 3 of the first somatosensory cortex of the conscious monkey. Exp. Brain Res. 5 1: 315-326, 1983. JENKINS, W. M. AND MERZENICH, M. M. Reorganization of neocortical representations after brain injury: a neurophysiological model of the bases of recovery from stroke. In: Progress in Brain Research, edited by F. J. Seil, E. Herbert, and B. M. Carlson. Amsterdam: Elsevier, 1987, vol. 7 1, p. 249-266. JENKINS, W. M., MERZENICH, M. M., OCHS, M. T., ALLARD, T., AND Gu~c-ROBLES, E. Functional reorganization of primary somatosensory cortex in adult owl monkeys after behaviorally controlled tactile stimulation. J. Neurophysiol. 63: 82- 104, 1990. KAAS, J. H., NELSON, R. J., SUR, M., AND MERZENICH, M. M. The postcentral somatosensory cortex: multiple representations of the body in primates. In: Cortical Sensory Organization. Multiple Somatic Areas, edited by C. N. Woolsey. Clifton, NJ: Humana, 198 1, vol. 1, p. 23-36. KALASKA, J. AND POMEIUNZ, B. Chronic paw denervation causes an agedependent appearance of novel responses from forearm in “paw cortex” of kittens and adult cats. J. Neurophysiol. 42: 6 18-633, 1979. KELEHAN, A. M. AND DOETSCH, G. S. Time-dependent changes in the functional organization of somatosensory cerebral cortex following digit amputation in adult raccoons. Somatosens. Res. 2: 49-8 1, 1984. KOSAR, E. AND HAND, P. J. First somatosensory cortical columns and associated neuronal clusters of nucleus ventralis and posterolateralis of the cat: an anatomical demonstration. J. Comp. Neural. 198: 5 15-539, 1981. KRISHNAMURTI, A., SANIDES, F., AND WELKER, W. I. Microelectrode mapping of modality-specific somatic sensory cerebral neocortex in slow loris. Brain Behav. Evol. 13: 267-283, 1976. LANDRY, P. AND DESCH~NES, M. Intracortical arborizations and receptive fields of identified ventrobasal thalamocortical afferents to the primary somatic sensory cortex in the cat. J. Comp. Neurol. 199: 345-37 1, 1981. LASHLEY, K. S. The problem of serial order in behavior. In: CerebraZMechanisms in Behavior, edited by L. A. Jeffress. New York: Wiley, 195 1, p. 112-136. MACGILLIS, M., KANG, R., AND ZARZECKI, P. Interactions among convergent inputs to somatosensory cortex neurons. Brain Res. 276: 329-332, 1983. MERZENICH, M. M. Sources of intraspecies and interspecies cortical map variability in mammals: conclusions and hypotheses. In: Comparative Neurobiology: Modes of Communication in the Nervous System, edited by G. M. Edelman, W. E. Gall, and W. M. Cowan. New York: Wiley, 1985, p. 138-157. MERZENICH, M. M. Dynamic neocortical processes and the origins of higher brain functions. In: The Neural and Molecular Bases of Learning, edited by J.-P. Changeux and M. Konishi. London: Wiley, 1987, p. 337-358. MERZENICH, M. M., JENKINS, W. M., AND MIDDLEBROOKS, J. C. Observations and hypotheses on special organizational features of the central auditory nervous system. In: Dynamic Aspects of Neocortical Function, edited by G. M. Edelman, E. Gall, and W. M. Cowan. New York: Wiley, 1984a, p. 397-424. MERZENICH, M. M., KAAS, J. H., SUR, M., AND LIN, C.-S. Double representation of the body surface within cytoarchitectonic areas 3b in “S-I” in the owl monkey (Aotus trivirgatus). J. Comp. Neural. 18 1: 4 l-74, 1978. MERZENICH, M. M., KAAS, J. H., WALL, J. T., NELSON, R. J., SUR, M., AND FELLEMAN, D. J. Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience 8: 33-55, 1983a. MERZENICH, M. M., KAAS, J. H., WALL, J. T., SUR, M., NELSON, R. J., AND FELLEMAN, D. J. Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys. Neuroscience 10: 639-665, 1983b. MERZENICH, M. M., NELSON, R. J., KAAS, J. H., STRYKER, M. P., JENKINS, W. M., ZOOK, J. M., CYNADER, M. S., AND SCHOPPMANN, A. Variability in hand surface representations in areas 3b and 1 in adult owl and squirrel monkeys. J. Comp. Neural. 258: 28 i-297, 1987. MERZENICH, M. M., NELSON, R. J., STRYKER, M. S., CYNADER, M. S., HICKS,
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SCHOPPMANN, A., AND ZOOI& J. M. Somatosensory cortical map changes following digit amputation in adult monkeys. J. Camp. Neural. 224: 59 l-605, 1984b. MERZENICH, M. M., RECANZONE, G. H., JENKINS, W. M., ALLARD, T., AND NUDO, R. J. Cortical representational plasticity. In: Neurobiology of the Neocortex. Dahlem Konferenzen, edited by P. Rakic and W. Singer. New York: Wiley, 1988, p. 4 l-67. MEFUENICH, M. M., SUR, M., NELSON, R. J., AND KAAS, J. H. Organization of the SI cortex: multiple cutaneous representations in areas 3b and 1 of the owl monkey. In: Cortical Sensory Organization. Multiple Somatic Areas, edited by C. N. Woolsey. Clifton, NJ: Humana, 198 1, vol. 1, p. 36-48. NELSON, R. J., SUR, M., FELLEMAN, D. J., AND KAAS, J. H. Representations of the body surface in postcentral parietal cortex of Macacafascicularis. J. Comp. Neural. 192: 6 1 l-643, 1980. PAUL, R. L., MERZENICH, M. M., AND GOODMAN, H. Representation of slowly and rapidly adapting cutaneous mechanoreceptors of the hand in Brodmann’s areas 3 and 1 of Macaca mulatta. Brain Rex 36: 229-249, 1972. PONS, T. P., GARRAGHTY, P. E., AND MISHKIN, M. Lesion-induced plasticity in the second somatosensory cortex of adult macaques. Proc. Natl. Acad. Sci. USA 85: 5279-528 1, 1988. PONS, T. P., WALL, J. T., GARRAGHTY, P. E., CUSICK, C. G., AND KAAS, J. H. Consistent features in the representation of the hand in area 3b of macaque monkeys. Somatosens. Res. 4: 309-33 1, 1987. POWELL, T. P. S. AND MOUNTCASTLE, V. B. Some aspects of the functional organization of the cortex of the postcentral gyrus of the monkey. A correlation of findings obtained in a single unit analysis with cytoarchitecture. Bull. Johns Hopkins Hosp. 105: 133-162, 1959. RASMUSSON, D. D. Reorganization of raccoon somatosensory cortex following removal of the fifth digit. J. Comp. Neural. 205: 3 13-326, 1982. RECANZONE, G. H., ALLARD, T., JENKINS, W. M., AND MERZENICH, M. M. Receptive field changes induced by peripheral nerve stimulation in SI of adult cats. J. Neurophysiof. 63: 12 13- 1225, 1990.
AND MERZENICH
G. H. AND MERZENICH, M. M. Intracortical microstimulation in somatosensory cortex in adult rats and owl monkeys results in a large expansion of the cortical zone of representation of a specific cortical receptive field. Sot. Neurosci. Abstr. 14: 223, 1988. SNOW, P. J., NUDO, R. J., RIVERS, W. J., JENKINS, W. M., AND MERZENIGH, M. M. Somatotopically inappropriate projections from thalamocortical neurons to the S-I cortex of the cat demonstrated by the use of intracortical microstimulation. Somatosens. Res. 5: 349-372, 1988. STRYKER, M. P., JENKINS, W. M., AND MERZENICH, M. M. Anesthetic state does not affect the map of the hand representation within area 3b somatosensory cortex in owl monkey. J. Comp. Neural. 258: 297-303, 1987. SUR, M., MERZENICH, M. M., AND KAAS, J. H. Magnification, receptive field area and “hypercolumn” size in areas 3b and 1 of somatosensory cortex in owl monkeys. J. Comp. Neural. 44: 295-3 11, 1980. SUR, M., NELSON, R. J., AND KAAS, J. H. Representations of the body surface in cortical areas 3b and 1 of squirrel monkeys: comparisons with other primates. J. Camp. Neural. 2 11: 177-l 92, 1982. WALL, J. T. AND CUSICK, C. G. Cutaneous responsiveness in primary somatosensory (SI) hindpaw cortex before and after partial hindpaw deafferentiation in adult rats. J. Neurosci. 4: 1499- 15 15, 1984. WALL, J. T. AND CUSICK, C. G. The representation of peripheral nerve inputs in the S- 1 hindpaw cortex of rats raised with incompletely innervated hindpaws. J. Neurosci. 67: I 129-l 147, 1986. WARREN, S. AND CARLSON, M. Organization of cutaneous input from hand to primary somatic sensory (SI) hand area in an old world primate, Erythrocebus patas. Sot. Neurosci. Abstr. 13: 250, 1987. ZARZECKI, P., BLUM, P. S., BAKKER, D. S., AND HERMAN, D. Convergence of sensory inputs upon projection neurons of somatosensory cortex: vestibular, neck, head, and forelimb inputs. Exp. Brain Res. 50: 408414, 1983. ZARZECKI, P. AND WIGGIN, D. M. Convergence of sensory inputs upon projection neurons of somatosensory cortex. Exp. Brain Res. 48: 28-42, 1982. RECANZONE,
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Reorganization of Somatosensory Area 3b Representations in Adult Owl Monkeys After Digital Syndactyly T. ALLARD, S. A. CLARK, W. M. JENKINS, AND M. M. MERZENICH Departments of Otolaryngology and Physiology, University of California at San Francisco Medical Center, San Francisco, California 94143
SUMMARY
AND
CONCLUSIONS
1. These experiments were designed to test the hypothesis that temporally correlated afferent input activity plays a lifelong role in the establishment and modification of receptive fields (RFs) and representational topographies in the primary somatosensory cortex of adult monkeys. They were based in part on the finding that adjacent digits of the hand are represented discontinuously in area 3b of the adult owl monkey. If cortical receptive fields and the details of cortical topographic representations are shaped by the weights of the temporal correlations among afferent inputs, then representational discontinuities between digits would be expected to arise because inputs from the skin surfacesof adjacent digits are largely independent in the critical time domain. 2. In the present experiments, the skin of adjacent digits 3 and 4 of the monkey hand was surgically connected to create an artificial syndactyly, or webbed-finger condition. Highly detailed microelectrode maps of the cortical representation of the syndactyl digits were obtained 3-7.5 mo later. This experimental manipulation greatly increased the amount of simultaneous or nearly simultaneous input from the normally separated, now fused, surfaces of adjacent fingers. 3. Cortical maps of the representations of finger surfaces were highly modified from the normal after a several-month-long period of digital fusion. Specifically, the normal discontinuity between the cortical representations of adjacent fingers was abolished. Within a wide cortical zone, RFs were defined that extended acrossthe line of syndactyly onto the surgically joined skin of both fused digits. The representational topography of the fused digits was similar to any normal single digit and was characterized by a continuous progression of partially overlapping RFs. 4. Control observations revealed that these reorganizational changes cannot be accounted for by any changes in cutaneous innervation induced by the surgery. They must arise from representational changes in the central somatosensory system. 5. These findings reveal that cortical maps can be altered in detail in adult monkeys by modifying the distributed temporal structure of afferent inputs. They support the longstanding hypothesis that the temporal coincidence of inputs plays a role in the grouping of input subsets into specific cortical RFs and, consequently, in the shaping of selected effective cortical inputs and representational topographies throughout life. INTRODUCTION
Recent electrophysiological experiments conducted within primary somatosensory cortical (SI) fields in adult rats, cats, raccoons, and monkeys have shown that the topographic cortical representations of the skin surfaces within these zones can be substantially altered after peripheral denervation (Dykes and Lamour 1988; Franck 1980; Kalaska 1048
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and Pomeranz 1979; Kelehan and Doetsch 1984; Merzenich et al. 1983a,b, 1984b; Rasmusson 1982; Wall and Cusick 1984, 1986), after differential use of limited skin surfaces in a behavioral task (Jenkins et al. 1990; Merzenich et al. 1988), or after restricted cortical lesions (Jenkins and Merzenich 1987; Pons et al. 1988). Throughout the lifespan of an adult mammal, somatosensory receptive fields (RFs) for neurons at specific cortical sites can enlarge or contract, and the cutaneous locations of their RFs can shift relatively long distances over the skin (see Merzenich 1985, 1987; Merzenich et al. 1984a, 1988 for review). Throughout these different reorganizational sequelae, a basic plan of local topography is usually conserved that is characterized by partially overlapping RFs defined at neighboring loci across the cortical surface (Jenkins and Merzenich 1987; Jenkins et al. 1990; Merzenich et al. 1983a,b, 1984b). We have previously argued that this dynamic representational remodeling might be accounted for by changes in the effectiveness of existing cortical synapses (Merzenich 198 5, 1987; Merzenich et al. 1984a, 1988). Thus reconstructed thalamic arbors extend beyond physiologically identified target zones in the more refined cortical map (Garraghty and Sur 1990; Kosar and Hand 198 1; Landry and Deschenes 198 1; Snow et al. 1988), cortical RFs rapidly enlarge severalfold in extent after topical administration of bicuculline (Dykes et al. 1984; Hicks and Dykes 1983) or after peripheral nerve stimulation (Recanzone et al. 1990), and excitatory postsynaptic potentials can be evoked in cortical neurons from skin sources far beyond those that effectively drive them under natural stimulation (Macgillis et al. 1983; Zarzecki et al. 1983; Zarzecki and Wiggin 1982). These and other data indicate that the specific subset of inputs comprising a cortical RF at a specific time in the life of an adult mammal is dynamically selected from a far larger array of anatomically existing inputs (Edelman 198 1; Edelman and Finkel 1984; Merzenich 1985, 1987; Merzenich et al. 1984a, 1988). Neurons at any given cortical location can be driven by many different combinations of inputs, comprising hundreds to thousands of different RFs at different times in a lifetime. Given this marked lifelong representational dynamism, what mechanisms underlie the process by which specific inputs are grouped into cortical RFs at any given time? What is the basis for the partially shifted RF overlap at neighboring cortical loci that is characteristic of topography in area 3b of SI? We have earlier hypothesized that this process of input selection is based on the temporal synchro-
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Physiological
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nization of inputs and on a system of horizontal network influences by which inputs at any given location influence inputs selected by their neighbors (Merzenich 1985, 1987; Merzenich et al. 1984a). The present experiments are designed to provide a simple test of this hypothesis. In normal adult owl monkeys, individual digits are represented in a segregated fashion in cortical area 3b. The skin of adjacent digits is represented in discrete cortical zones with abrupt borders, differentiating one digit’s representation from its neighboring digit’s representation. On either side of these representational discontinuities, neurons usually are driven exclusively by stimulation of one or the other of the two bordering digits. That is, RFs are almost always restricted to single digits. According to our hypothesis, the cortical representations of individual adjacent digits are not segregated by their anatomic connections, but because the activity of peripheral inputs from the independent skin surfaces of adjacent fingers is relatively poorly correlated in the critical time domain (tens of milliseconds). In support of this claim, we have already demonstrated that anatomic inputs from single thalamic neurons in the cat commonly project across the lines of representational discontinuities in the cortex (Snow et al. 1988) and that, in many representational remodeling experiments in monkeys, discontinuities between the representation of digits appear to move long distances across the cortex (Jenkins and Merzenich 1987; Merzenich et al. 1983a,b) and to reform between newly apposed digits after amputation (Merzenith et al. 1984b). These studies strongly indicate that the recorded representational discontinuities in cortical maps are functional, and not anatomic, entities. If that is the case, and if input selection and topographies are based on the temporal coincidence of afferent inputs, then discontinuities in representation between digits in monkeys should be abolished by increasing the temporal coactivation of inputs from adjacent fingers, thereby creating a large pool of potential RFs combining inputs from both digits. Increased coactivation of inputs from adjacent fingers can be achieved by mechanically coupling the skin surfaces of those digits surgically, thereby creating an artificial syndactyly, or webbed-finger condition. This fusion of the skin of the two digits should result in temporally synchronous stimulation across the newly adjoined skin, much like that normally occurring across a single digit. In these studies, consistent with our hypothesis, fusion of two adjacent digits resulted in a disappearance of the normal discontinuity between digit representations and the emergence of a broad region of cortex with single-component RFs combining inputs from both syndactyl digits. Preliminary reports of these results have been published earlier (Allard et al. 1985; Clark et al. 1988). METHODS
The dorsal and volar skin of digits 3 and 4 of the hands of adult owl monkeys (Aotus nancymai) were surgically connected from distal to proximal phalanges, creating syndactyl fingers in three intensively studied cases.After 14, 25, or 33 wk, a single, highly detailed map of the cutaneous representation of these digits and adjacent skin surfaces was obtained in the primary koniocortical SI field, area 3b, in each case.Similarly detailed cortical maps have
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also been derived in a series of normal (control) monkeys (Merzenith et al. 1987; Stryker et al. 1987). Peripheral hand surgeries All initial hand surgeries were conducted under sterile conditions and with the use of conventional human surgical procedures by an experienced surgeon with expertise in human plastic surgery and microsurgery (S. A. Clark). General anesthesia was induced and maintained by the use of halothane (l-2%) in a nitrous oxide (1.5 l/min)-oxygen (0.5 l/min) mixture. Core body temperature was monitored and maintained at 375°C with a feedback-controlled heating pad. The arm was exsanguinated with a tourniquet following conventional human protocols. Incisions were made with the aid of a surgical microscope along the midlateral lines of ulnar digit 3 and radial digit 4. This line sharply demarcates the limits of distribution of the digital cutaneous nerves innervating volar glabrous and dorsal hairy digital skin. Dorsal and volar skin flaps were sewn together along their entire lengths with 8-O vycril suture on a microsurgical needle to minimize tissue trauma. Total tourniquet time was 2 mm in cats and monkeys (Garraghty and Sur 1990; Kosar and Hand 198 1; Landry and Deschenes 198 1; Snow et al. 1988), and inputs from even more distant peripheral sources can evoke excitatory postsynaptic potentials in cortical neurons (Macgillis et al. 1983; Zarzecki et al. 1983; Zarzecki and Wiggin 1982). On the other hand, it is not clear why normal distance limits are exceeded in these fused-digit cases or why persistent patches representing skin along the scar line can be found throughout the zone of representation of digits 3 and 4. In a normal map of a sinDORSAL DIGIT REPRESENTATION. gle digit, the representation of the glabrous skin is often a contiguous uninterrupted patch that is bordered in some places by the representation of hairy skin. In the present series, the fused glabrous representation of digits 3 and 4 was partially interrupted in each case by a large central patch of hairy skin representation. This segregated patch of dorsal representation on the middle and proximal phalanges was completely surrounded by glabrous RFs representing the skin of the fused digits. This central patch of hairy skin representation may have existed in the same position before the surgical syndactyly. If this were the case, the dorsal patch would serve as a marker of the original abrupt discontinuity between digits 3 and 4 that must have existed before the syndactyly surgery was performed. Under these circumstances, the emergence of universally double-digit dorsal fields would merely reflect the changing temporal structure of their original driving inputs. Alternatively, other factors associated with the syndactyly itself could induce the formation of a dorsal patch of double-digit RFs at a point in the cortical zone intermediate between the normal representation of digits 3 and 4. Some inputs from the radial nerve supplying the dorsum of the hand are actively suppressed in the central representation of the glabrous hand (Merzenich et al. 1983a,b); median nerve section produces an immediate unmasking of hairy inputs to the hand region in area 3b of adult owl monkeys. It is possible that a dorsal representation could emerge within a formerly glabrous region, exploiting existing but suppressed inputs from the hairy skin. NONCONTIGUOUS RFs. Noncontiguous double-digit RFs occurred at the distal tips of digits 3 and 4. These dual-component RFs almost certainly reflect the consequences of central reorganization, rather than abnormal peripheral innervation (see above). Noncontiguous fields were not found in a segregated topographic region, but they did respect the general plan of proximal-to-distal organization in the syndactyly zone. It appears likely that the temporal synchronization of afferent inputs is a principal factor that determines which input combinations contribute to RFs. The emergence of these noncontiguous RFs provides evidence that there is no a priori requirement that afferent inputs selected to gener-
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ate given RFs be continuous. If this is the case, then why are neighboring RFs normally continuous, as a rule? We hypothesize that normal RF structure simply manifests the fact that incident stimulation of the skin results in costimulation at distant or separated skin locations with low probability. By contrast, immediately adjacent neighboring skin locations that are mechanically coupled have a relatively higher probability of coincident or correlated stimulation. This hypothesis is subject to simple experimental testing now being initiated in our laboratory. We thank G. Recanzone and R. Nudo for important technical advice and assistance. This research was supported by National Institute of Neurological Disorders and Stroke Grant NS- 104 14, the John C. and Edward Coleman Memorial Fund, and Hearing Research. Address for reprint requests: T. Allard, Cognitive and Neural Sciences (1142), Office of Naval Research, 800 N. Quincy St., Arlington, VA 222 175000. Received 26 July 1988; accepted in final form 25 April 199 1. REFERENCES T. Biological constraints on a dynamic network: the somatosensory system. In: Connectionist Modeling and Brain Function: The Developing Interface, edited by S. J. Hanson and C. Olson. Cambridge, MA: MIT Press, 1990, p. 132- 163. ALLARD, T., CLARK, S. A., JENKINS, W. M., AND MEFUENICH, M. M. Syndactyly results in the emergence of double-digit receptive fields in somatosensory cortex in adult owl monkeys. Sot. Neurosci. Abstr. 11: 965, 1985. ALLOWAY, K. D., SINCLAIR, R. J., AND BURTON, H. Responses of neurons in somatosensory cortical area II of cats to high frequency vibratory stimulation during iontophoresis of a GABA antagonist and glutamate. Somatosens. Mot. Res. 6: 109- 140, 1988. CALFORD, M. B. AND TWEEDALE, R. Immediate and chronic changes in responses of somatosensory cortex in adult flying-fox after digit amputation. Nature Lond. 332: 446-448, 1988. CLARK, S. A., ALLARD, T., JENKINS, W. M., AND MERZENICH, M. M. Receptive fields in the body-surface map in adult cortex defined by temporally correlated inputs. Nature Lond. 332: 444-445, 1988. DYKES, R. W. AND LAMOUR, Y. An electrophysiological laminar analysis of single somatosensory neurons in partially deafferented rat hindlimb granular cortex subsequent to transection of the sciatic nerve. Brain Res. 449: 1-17, 1988. DYKES, R. W., LANDRY, P., METHERATE, R., AND HICKS, T. P. Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons. J. Neurophysiol. 52: 1066- 1093, 1984. EDELMAN, G. M. Group selection as the basis for higher brain function. In: Organization of the Cerebral Cortex, edited by F. 0. Schmitt, F. G. Worden, G. Adelman, and S. G. Dennis. Cambridge, MA: MIT Press, 1981, p. 51-100. EDELMAN, G. M. AND FINKEL, L. H. Neuronal group selection in the cerebral cortex. In: Dynamic Aspects of Neocortical Function, edited by G. M. Edelman, W. E. Gall, and W. M. Cowan. New York: Wiley, 1984, p. 653-695. FRANCK, J. I. Functional reorganization of cat somatic sensory-motor cortex (SmI) after selective dorsal root rhizotomies. Brain Res. 186: 458462, 1980. GARDNER, E. P. Somatosensory cortical mechanisms of feature detection in tactile and kinesthetic discrimination. Can. J. Physiol. Pharmacol. 66: 439-454, 1988. GARRAGHTY, P. E., PONS, T. P., SUR, M., AND KAAS, J. H. The arbors of axon terminations in middle cortical layers of somatosensory area 3b in owl monkeys. Somatosens. Mot. Res. 6: 40 l-4 11, 1989. GARRAGHTY, P. E. AND SUR, M. Morphology of single intracellularly stained axons terminating in area 3b of macaque monkeys. J. Comp. Neural. 294: 583-593, 1990. HEBB, D. 0. The Organization of Behavior. New York: Wiley, 1949. ALLARD,
FUSION
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T. P. AND DYKES, R. P. Receptive field size for certain neurons in primary somatosensory cortex is determined by GABA-mediated intracortical inhibition. Brain Res. 274: 160- 164, 1983. IWAMURA, Y., TANAKA, M., SAKAMOTO, M., AND HIKOSAKA, 0. Functional subdivisions representing different finger regions in area 3 of the first somatosensory cortex of the conscious monkey. Exp. Brain Res. 5 1: 315-326, 1983. JENKINS, W. M. AND MERZENICH, M. M. Reorganization of neocortical representations after brain injury: a neurophysiological model of the bases of recovery from stroke. In: Progress in Brain Research, edited by F. J. Seil, E. Herbert, and B. M. Carlson. Amsterdam: Elsevier, 1987, vol. 7 1, p. 249-266. JENKINS, W. M., MERZENICH, M. M., OCHS, M. T., ALLARD, T., AND Gu~c-ROBLES, E. Functional reorganization of primary somatosensory cortex in adult owl monkeys after behaviorally controlled tactile stimulation. J. Neurophysiol. 63: 82- 104, 1990. KAAS, J. H., NELSON, R. J., SUR, M., AND MERZENICH, M. M. The postcentral somatosensory cortex: multiple representations of the body in primates. In: Cortical Sensory Organization. Multiple Somatic Areas, edited by C. N. Woolsey. Clifton, NJ: Humana, 198 1, vol. 1, p. 23-36. KALASKA, J. AND POMEIUNZ, B. Chronic paw denervation causes an agedependent appearance of novel responses from forearm in “paw cortex” of kittens and adult cats. J. Neurophysiol. 42: 6 18-633, 1979. KELEHAN, A. M. AND DOETSCH, G. S. Time-dependent changes in the functional organization of somatosensory cerebral cortex following digit amputation in adult raccoons. Somatosens. Res. 2: 49-8 1, 1984. KOSAR, E. AND HAND, P. J. First somatosensory cortical columns and associated neuronal clusters of nucleus ventralis and posterolateralis of the cat: an anatomical demonstration. J. Comp. Neural. 198: 5 15-539, 1981. KRISHNAMURTI, A., SANIDES, F., AND WELKER, W. I. Microelectrode mapping of modality-specific somatic sensory cerebral neocortex in slow loris. Brain Behav. Evol. 13: 267-283, 1976. LANDRY, P. AND DESCH~NES, M. Intracortical arborizations and receptive fields of identified ventrobasal thalamocortical afferents to the primary somatic sensory cortex in the cat. J. Comp. Neurol. 199: 345-37 1, 1981. LASHLEY, K. S. The problem of serial order in behavior. In: CerebraZMechanisms in Behavior, edited by L. A. Jeffress. New York: Wiley, 195 1, p. 112-136. MACGILLIS, M., KANG, R., AND ZARZECKI, P. Interactions among convergent inputs to somatosensory cortex neurons. Brain Res. 276: 329-332, 1983. MERZENICH, M. M. Sources of intraspecies and interspecies cortical map variability in mammals: conclusions and hypotheses. In: Comparative Neurobiology: Modes of Communication in the Nervous System, edited by G. M. Edelman, W. E. Gall, and W. M. Cowan. New York: Wiley, 1985, p. 138-157. MERZENICH, M. M. Dynamic neocortical processes and the origins of higher brain functions. In: The Neural and Molecular Bases of Learning, edited by J.-P. Changeux and M. Konishi. London: Wiley, 1987, p. 337-358. MERZENICH, M. M., JENKINS, W. M., AND MIDDLEBROOKS, J. C. Observations and hypotheses on special organizational features of the central auditory nervous system. In: Dynamic Aspects of Neocortical Function, edited by G. M. Edelman, E. Gall, and W. M. Cowan. New York: Wiley, 1984a, p. 397-424. MERZENICH, M. M., KAAS, J. H., SUR, M., AND LIN, C.-S. Double representation of the body surface within cytoarchitectonic areas 3b in “S-I” in the owl monkey (Aotus trivirgatus). J. Comp. Neural. 18 1: 4 l-74, 1978. MERZENICH, M. M., KAAS, J. H., WALL, J. T., NELSON, R. J., SUR, M., AND FELLEMAN, D. J. Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience 8: 33-55, 1983a. MERZENICH, M. M., KAAS, J. H., WALL, J. T., SUR, M., NELSON, R. J., AND FELLEMAN, D. J. Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys. Neuroscience 10: 639-665, 1983b. MERZENICH, M. M., NELSON, R. J., KAAS, J. H., STRYKER, M. P., JENKINS, W. M., ZOOK, J. M., CYNADER, M. S., AND SCHOPPMANN, A. Variability in hand surface representations in areas 3b and 1 in adult owl and squirrel monkeys. J. Comp. Neural. 258: 28 i-297, 1987. MERZENICH, M. M., NELSON, R. J., STRYKER, M. S., CYNADER, M. S., HICKS,
Downloaded from www.physiology.org/journal/jn by ${individualUser.givenNames} ${individualUser.surname} (163.015.154.053) on November 25, 2018. Copyright © 1991 the American Physiological Society. All rights reserved.
1058
ALLARD,
CLARK,
JENKINS,
SCHOPPMANN, A., AND ZOOI& J. M. Somatosensory cortical map changes following digit amputation in adult monkeys. J. Camp. Neural. 224: 59 l-605, 1984b. MERZENICH, M. M., RECANZONE, G. H., JENKINS, W. M., ALLARD, T., AND NUDO, R. J. Cortical representational plasticity. In: Neurobiology of the Neocortex. Dahlem Konferenzen, edited by P. Rakic and W. Singer. New York: Wiley, 1988, p. 4 l-67. MEFUENICH, M. M., SUR, M., NELSON, R. J., AND KAAS, J. H. Organization of the SI cortex: multiple cutaneous representations in areas 3b and 1 of the owl monkey. In: Cortical Sensory Organization. Multiple Somatic Areas, edited by C. N. Woolsey. Clifton, NJ: Humana, 198 1, vol. 1, p. 36-48. NELSON, R. J., SUR, M., FELLEMAN, D. J., AND KAAS, J. H. Representations of the body surface in postcentral parietal cortex of Macacafascicularis. J. Comp. Neural. 192: 6 1 l-643, 1980. PAUL, R. L., MERZENICH, M. M., AND GOODMAN, H. Representation of slowly and rapidly adapting cutaneous mechanoreceptors of the hand in Brodmann’s areas 3 and 1 of Macaca mulatta. Brain Rex 36: 229-249, 1972. PONS, T. P., GARRAGHTY, P. E., AND MISHKIN, M. Lesion-induced plasticity in the second somatosensory cortex of adult macaques. Proc. Natl. Acad. Sci. USA 85: 5279-528 1, 1988. PONS, T. P., WALL, J. T., GARRAGHTY, P. E., CUSICK, C. G., AND KAAS, J. H. Consistent features in the representation of the hand in area 3b of macaque monkeys. Somatosens. Res. 4: 309-33 1, 1987. POWELL, T. P. S. AND MOUNTCASTLE, V. B. Some aspects of the functional organization of the cortex of the postcentral gyrus of the monkey. A correlation of findings obtained in a single unit analysis with cytoarchitecture. Bull. Johns Hopkins Hosp. 105: 133-162, 1959. RASMUSSON, D. D. Reorganization of raccoon somatosensory cortex following removal of the fifth digit. J. Comp. Neural. 205: 3 13-326, 1982. RECANZONE, G. H., ALLARD, T., JENKINS, W. M., AND MERZENICH, M. M. Receptive field changes induced by peripheral nerve stimulation in SI of adult cats. J. Neurophysiof. 63: 12 13- 1225, 1990.
AND MERZENICH
G. H. AND MERZENICH, M. M. Intracortical microstimulation in somatosensory cortex in adult rats and owl monkeys results in a large expansion of the cortical zone of representation of a specific cortical receptive field. Sot. Neurosci. Abstr. 14: 223, 1988. SNOW, P. J., NUDO, R. J., RIVERS, W. J., JENKINS, W. M., AND MERZENIGH, M. M. Somatotopically inappropriate projections from thalamocortical neurons to the S-I cortex of the cat demonstrated by the use of intracortical microstimulation. Somatosens. Res. 5: 349-372, 1988. STRYKER, M. P., JENKINS, W. M., AND MERZENICH, M. M. Anesthetic state does not affect the map of the hand representation within area 3b somatosensory cortex in owl monkey. J. Comp. Neural. 258: 297-303, 1987. SUR, M., MERZENICH, M. M., AND KAAS, J. H. Magnification, receptive field area and “hypercolumn” size in areas 3b and 1 of somatosensory cortex in owl monkeys. J. Comp. Neural. 44: 295-3 11, 1980. SUR, M., NELSON, R. J., AND KAAS, J. H. Representations of the body surface in cortical areas 3b and 1 of squirrel monkeys: comparisons with other primates. J. Camp. Neural. 2 11: 177-l 92, 1982. WALL, J. T. AND CUSICK, C. G. Cutaneous responsiveness in primary somatosensory (SI) hindpaw cortex before and after partial hindpaw deafferentiation in adult rats. J. Neurosci. 4: 1499- 15 15, 1984. WALL, J. T. AND CUSICK, C. G. The representation of peripheral nerve inputs in the S- 1 hindpaw cortex of rats raised with incompletely innervated hindpaws. J. Neurosci. 67: I 129-l 147, 1986. WARREN, S. AND CARLSON, M. Organization of cutaneous input from hand to primary somatic sensory (SI) hand area in an old world primate, Erythrocebus patas. Sot. Neurosci. Abstr. 13: 250, 1987. ZARZECKI, P., BLUM, P. S., BAKKER, D. S., AND HERMAN, D. Convergence of sensory inputs upon projection neurons of somatosensory cortex: vestibular, neck, head, and forelimb inputs. Exp. Brain Res. 50: 408414, 1983. ZARZECKI, P. AND WIGGIN, D. M. Convergence of sensory inputs upon projection neurons of somatosensory cortex. Exp. Brain Res. 48: 28-42, 1982. RECANZONE,
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