Somatosensory cortical map changes following digit amputation in adult monkeys

Journal of Comparative Neurology - Tập 224 Số 4 - Trang 591-605 - 1984
Michael M. Merzenich1,2, Randall J. Nelson3, Michael P. Stryker1, Max S. Cynader4, A. Schoppmann5, John M. Zook6
1Coleman Laboratory and the Departments of Physiology, University of California at San Francisco, San Francisco, California 94143
2Otolaryngology, University of California at San Francisco, San Francisco, California 94143
3Laboratory of Neurophysiology, NIMH, Bethesda, Maryland 20205
4Department of Psychology, Dalhousie University, Halifax, Nova Scotia, B3H 4J1, Canada
5Abt. Biologie IV, Universitat-Oberer Eselsberg, 7900 ULM/Donau, West Germany
6Department of Zoological and Biomedical Science, Ohio University, Athens, Ohio 45701

Tóm tắt

Abstract

The cortical representations of the hand in area 3b in adult owl monkeys were defined with use of microelectrode mapping techniques 2–8 months after surgical amputation of digit 3, or of both digits 2 and 3. Digital nerves were tied to prevent their regeneration within the amputation stump. Successive maps were derived in several monkeys to determine the nature of changes in map organization in the same individuals over time.

In all monkeys studied, the representations of adjacent digits and palmar surfaces expanded topographically to occupy most or all of the cortical territories formerly representing the amputated digit(s). With the expansion of the representations of these surrounding skin surfaces (1) there were severalfold increases in their magnification and (2) roughly corresponding decreases in receptive field areas. Thus, with increases in magnification, surrounding skin surfaces were represented in correspondingly finer grain, implying that the rule relating receptive field overlap to separation in distance across the cortex (see Sur et al., '80) was dynamically maintained as receptive fields progressively decreased in size.

These studies also revealed that: (1) the discontinuities between the representations of the digits underwent significant translocations (usually by hundreds of microns) after amputation, and sharp new discontinuous boundaries formed where usually separated, expanded digital representations (e.g., of digits 1 and 4) approached each other in the reorganizing map, implying that these map discontinuities are normally dynamically maintained. (2) Changes in receptive field sizes with expansion of representations of surrounding skin surfaces into the deprived cortical zone had a spatial distribution and time course similar to changes in sensory acuity on the stumps of human amputees. This suggests that experience‐dependent map changes result in changes in sensory capabilities. (3) The major topographic changes were limited to a cortical zone 500–700 μm on either side of the initial boundaries of the representation of the amputated digits. More distant regions did not appear to reorganize (i.e., were not occupied by inputs from surrounding skin surfaces) even many months after amputation. (4) The representations of some skin surfaces moved in entirety to locations within the former territories of representation of amputated digits in every monkey studied. In man, no mislocation errors or perceptual distortions result from stimulation of surfaces surrounding a digital amputation. This constitutes further evidence that any given skin surface can be represented by many alternative functional maps at different times of life in these cortical fields (Merzenich et al., '83b).

These studies further demonstrate that basic features of somatosensory cortical maps (receptive field sizes, cortical sites of representation of given skin surfaces, representational discontinuities, and probably submodality column boundaries) are dynamically maintained. They suggest that cortical skin surface maps are alterable by experience in adults, and that experience‐dependent map changes reflect and possibly account for concomitant changes in tactual abilities. Finally, these results bear implications for mechanisms underlying these cortical map dynamics.

Từ khóa


Tài liệu tham khảo

10.1002/cne.901350203

Carson L. V., 1982, Clinical Neurosurgery, 532

Clark W. E. L., 1957, On the thalamocortical connexions of the general sensory cortex of Macaca, Proc. R. Soc. Lond. [Biol.], 141, 467

Cotman C. W., 1982, Synapse turnover in adult vertebrates, Physiol. Rev., 61, 684, 10.1152/physrev.1981.61.3.684

Chronholm B., 1951, Phantom limb in amputees: Study of changes in integration of centripetal impulses with special references to referred sensations, Acta Psychiatr. Neurol. [Suppl.], 72, 1

10.1016/0014-4886(76)90219-3

10.1152/jn.1982.47.4.677

Dykes R. W., 1981, Magnification factors and organization of submodality‐specific bands in SI cortex of the cat, J. Compo Neurol., 202, 497, 10.1002/cne.902020411

Edelman G. M., 1982, The Organization of the Cerebral Cortex, 535

Edelman G. M., 1984, Dynamic Aspects of Neocortical Function

10.1080/00223980.1955.9712969

10.1111/j.1749-6632.1958.tb39524.x

10.1136/jnnp.11.2.88

Hebb D. O., 1949, Organization of Behavior

Jenkins W. M., 1982, The Area 3b representation of the hand in owl monkeys reorganizes after induction of restricted cortical lesions, Soc. Neurosci. Abstr., 8, 141

Katz D, 1920, Psychologische Versuche mit Amputierten, Tieren Z. Psychol. Physiol., 85, 32

Kelahan A. M., 1982, Functional organization of adult raccoon somatosensory cerebral cortex following neonatal digit amputation, Brain Res., 223, 152, 10.1016/0006-8993(81)90815-5

10.1007/BF00235250

10.1002/cne.901850209

Merrill E. G., 1978, Neuronal Plasticity, 94

10.1016/0166-2236(82)90235-1

10.1002/cne.901810104

Merzenich M. M., 1981, Cortical Sensory Organization, 36

10.1016/0306-4522(83)90024-6

10.1016/0306-4522(83)90208-7

Metzlar J., 1979, Functional changes in cat somatic sensory‐motor cortex during short‐term reversible epidermal blocks, Brain Res., 177, 379, 10.1016/0006-8993(79)90790-X

10.1016/0014-4886(76)90035-2

10.1152/jn.1957.20.4.408

Mountcastle V. B., 1979, The Neurosciences. Fourth Study Program, 21

Nelson R. J., 1981, Representations of the body surface in postcentral parietal cortex of Macaca fascicularis, Comp. Neurol., 192, 611, 10.1002/cne.901920402

10.1016/0304-3940(81)90270-6

10.1016/0006-8993(72)90732-9

Pons T., 1981, Axonal arborizations in area 3b of somatosensory cortex in the owl monkey, Aotus trivirgatus, Anat. Rec., 202, 151A

Ramón y Cajal S, 1911, Histologie du Système Nerveux de l'Homme et des Vertébrés

10.1002/cne.902050402

Scheibel M. E., 1970, The Neurosciences. Second Study Program, 443

Schoppmann A., 1981, Soc. Neurosci. Abstr., 7, 842

Stryker M. P. W. M.Jenkins andM. M.Merzenich(1984) Anesthetic state does not affect the map of the hand representation within area 3B somatosensory cortex in owl monkey.J. Comp. Neurol.(submitted).

Sur M.(1979) Some Principles of Organization of Somatosensory Cortex. Ph. D. Thesis Vanderbilt University Nashville.

Sur M., 1980, Magnification, receptive field area and “hypercolumn” size in Areas 3b and 1 of somatosensory cortex in owl monkeys, J. Compo Neurol., 44, 295

10.1126/science.7233199

Teuber H. L. H. P.Krieger andM. B.Bender(1948) Organization of sensorimotor functions following loss of limb. Unpublished manuscripted cited by Haber '55 '58.

Teuber H. L., 1949, Reorganization of sensory function in amputation stumps: Two‐point discrimination, Fed. Proc., 8, 156

Wall P. D., 1978, Physiology and Pathophysiology of Axons

10.1038/232542a0

10.1098/rspb.1976.0087