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Maintenance of a Somatotopic Cortical Map in the Face of Diminishing Thalamocortical Inputs (Plasticity͞divergence͞cortical Magnification)

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Maintenance of a Somatotopic Cortical Map in the Face of Diminishing Thalamocortical Inputs (Plasticity͞divergence͞cortical Magnification) Proc. Natl. Acad. Sci. USA Vol. 94, pp. 11003–11007, September 1997 Neurobiology Maintenance of a somatotopic cortical map in the face of diminishing thalamocortical inputs (plasticityydivergenceycortical magnification) E. G. JONES*, P. R. MANGER†, AND T. M. WOODS Department of Anatomy and Neurobiology, University of California, Irvine, CA 92697 Communicated by Vernon B. Mountcastle, Johns Hopkins University School of Medicine, Baltimore, MD, July 25, 1997 (received for review May 29, 1997) ABSTRACT This study addresses the extent of divergence of monkeys after making destructive lesions of increasing size in the ascending somatosensory pathways of primates. Diver- in parts of the thalamic representation of the hand. The results gence of inputs from a particular body part at each successive show that substantial parts of the thalamic representation of a synaptic step in these pathways results in a potential magni- finger can be removed before the representation of that finger fication of the representation of that body part in the somato- begins to shrink in the cortical somatotopic map. The degree sensory cortex, so that the representation can be expanded of divergence implied by these results is sufficiently great to when peripheral input from other parts is lost, as in nerve explain most cases of representational plasticity in the somato- lesions or amputations. Lesions of increasing size were placed sensory cortex even after substantial peripheral lesions. in the representation of a finger in the ventral posterior thalamic nucleus (VPL) of macaque monkeys. After a survival MATERIALS AND METHODS period of 1–5 weeks, area 3b of the somatosensory cortex ipsilateral to the lesion was mapped physiologically, and the Fifteen macaque monkeys (Macaca mulatta and Macaca nem- extent of the representation of the affected and adjacent estrina) were anesthetized with intramuscular ketamine and fingers was determined. Lesions affecting less than 30% of the maintained on a continuous intravenous infusion of Nembutal. thalamic VPL nucleus were without effect upon the cortical In 10, microelectrodes were introduced into one thalamus representation of the finger whose thalamic representation horizontally from behind, entering the thalamus via the visual was at the center of the lesion. Lesions affecting about 35% of cortex and midbrain. The ventral posterior lateral nucleus the VPL nucleus resulted in a shrinkage of the cortical (VPL) was identified, and receptive field mapping of single representation of the finger whose thalamic representation units and multiunit clusters responding to natural cutaneous was lesioned, with concomitant expansion of the representa- stimulation was used to isolate the extent of the representation tions of adjacent fingers. Beyond 35–40%, the whole cortical of a single finger (which normally occupies a more or less representation of the hand became silent. These results sug- parasagittal lamella, running on a curved trajectory through gest that divergence of brainstem and thalamocortical pro- the anteroposterior extent of VPL; Fig. 1A). Either a small jections, although normally not expressed, are sufficiently electrolytic lesion was made along the length of a large part of great to maintain a representation after a major loss of inputs this trajectory by passing 5–8 mA through the electrode as it from the periphery. This is likely to be one mechanism of was withdrawn or the recording electrode was replaced by a representational plasticity in the cerebral cortex. dual recordingyinjection cannula attached to a hydraulic de- livery system and 300 nl of 2 or 10 mM kainic acid (pH 3.5) was Plasticity of the body map in somatosensory cortex permits the injected along the trajectory representing a finger. Larger representation of a body part to expand or contract under the lesions were made by reintroducing the electrode or cannula influence of enhanced or reduced input from sensory recep- and making further electrolytic lesions or injections along tors of skin, muscle, and joints and probably underlies per- trajectories dorsal, ventral, medial, andyor lateral and parallel ceptual adaptations that occur during learning of new tactile to the first. skills (1) and after nerve injury (2) or amputation (3). The monkeys were allowed to recover; 1–5 weeks after Activity-dependent expansion of part of the body map in the lesioning, they were reanesthetized; and the representation of cerebral cortex at the expense of adjacent parts may depend the upper limb was mapped in area 3b of the somatosensory upon functional expression of divergent but previously sup- cortex ipsilateral to the lesion, by using the same single and pressed inputs from the periphery (4, 5) that reach the cortex multiunit recording of responses to peripheral stimulation as via the ventral posterior nucleus of the thalamus, upon long- for the thalamus. Microelectrodes were introduced at 200- to range intracortical connections (6), andyor upon sprouting of 500-mm intervals and were advanced down the posterior bank axons (5) in one or both pathways. of the central sulcus. Five normal monkeys in which the same The extent of thalamocortical divergence is a limiting factor area was mapped served as controls. At the conclusion of the in the potential for expansion of one representation at the cortical mapping, the animals were perfused with 4% para- expense of another (7–10). It can be magnified by similar formaldehyde in 0.1 M phosphate buffer (pH 7.4), the brains divergence of primary afferents to the dorsal column nuclei removed, infiltrated with sucrose, and frozen in dry ice. Serial and of dorsal column nuclear efferents to the ventral posterior frozen sections 30-mm thick were cut from the thalamus in the thalamic nucleus. The degree of this magnification has been frontal plane and from the cortex in the parasagittal plane. determined in the present study: the representation of the Alternate sections were stained with thionin, histochemically hand was mapped physiologically in the somatosensory cortex Abbreviations: VPL, ventral posterior lateral thalamic nucleus; VPM, The publication costs of this article were defrayed in part by page charge ventral posterior medial thalamic nucleus. *To whom reprint requests should be addressed. e-mail: egjones@ payment. This article must therefore be hereby marked ‘‘advertisement’’ in uci.edu. accordance with 18 U.S.C. §1734 solely to indicate this fact. †Present address: Neurobiology Research 151A3, Sepulveda Veterans’ © 1997 by The National Academy of Sciences 0027-8424y97y9411003-5$2.00y0 Administration Medical Center, 16111 Plummer Street, North Hills, PNAS is available online at http:yywww.pnas.org. CA 91343. 11003 Downloaded by guest on September 30, 2021 11004 Neurobiology: Jones et al. Proc. Natl. Acad. Sci. USA 94 (1997) FIG.1. (A) Representation of the body surface in the normal macaque monkey at a single coronal level of the ventral posterior nucleus (redrawn from ref. 11). The representation of a finger runs in a curved lamella through the full anteroposterior extent of the VPL nucleus. (B–D) Lesions of various sizes in cytochrome oxidase-stained sections from different monkeys. The lesions were made electrolytically along the length of the trajectory representing a finger. All lesions resulted in a reduction of immunostaining for the calcium binding protein parvalbumin (25) in a localized part of the layer IV plexus in area 3b (see Fig. 3C), its size proportional to the size of the thalamic lesion, indicating a loss of thalamocortical fibers. for cytochrome oxidase, or immunocytochemically for the other fingers occupies somewhat less (11). The curving nature calcium binding protein parvalbumin. of the representations makes it impossible for any small lesions Camera-lucida drawings were made of the Nissl- and cyto- made in the present manner to occupy the representation of chrome oxidase-stained sections through the thalamus, show- one finger throughout its full antero-posterior extent. All ing the extent of the lesion and its relationship to the borders lesions resulted in a reduction of immunostaining for parval- of VPL; the volume of VPL occupied by the lesion was bumin in a localized part of the layer IV plexus in area 3b (Fig. calculated. Nissl-stained sections of the cortex were used to 3C), its size proportional to the size of the thalamic lesion, locate microelectrode tracks in relation to the cytoarchitecture indicating a loss of thalamocortical fibers. of area 3b of the somatosensory cortex, and a map of the hand Small cylindrical lesions 0.5–1 mm in diameter that ran and adjacent parts of the upper limb representation was anteroposteriorly through the thalamus affecting over much of generated on the flattened cortex, by relating electrode tracks their length part of the representation of a single finger (11) to receptive field data collected during the terminal experi- were without effect on the cortical map in area 3b (Fig. 3A). ment. The sections stained immunocytochemically for parv- In these cases, a complete cortical representation of the finger albumin were used to identify regions of area 3b in which the was found, its internal topography was intact, and the size of layer IV plexus of parvalbumin-stained thalamocortical fibers the representation (2.5–10 mm2) was similar to that found in was deficient. the control monkeys (see also ref. 12). Receptive fields of neurons within the finger representation were identical in size RESULTS to those in normal monkeys and their responsiveness to stimuli was indistinguishable from those of normal monkeys within the Electrolytic or kainic acid lesions resulted in the destruction of limitations of the experimental setup. thalamic cells over a region whose size was related to the Lesions centered in the representation of a single finger amount of current passed or volume of excitotoxin injected. were without effect upon the cortical representation of that The lesioned area was distinguishable by loss of Nissl or finger until approximately 30% of the volume of VPL was cytochrome oxidase staining in the histological sections destroyed (Figs. 2 and 3B).
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