Preston Garraghty

After limited sensory deafferentations in adult primates, somatosensory cortical maps reorganize over a distance of 1 to 2 millimeters mediolaterally, that is, in the dimension along which different body parts are represented. This amount of reorganization was considered to be an upper limit imposed by the size of the projection zones of individual thalamocortical axons, which typically also extend a mediolateral distance of 1 to 2 millimeters. However, after extensive long-term deafferentations in adult primates, changes in cortical maps were found to be an order of magnitude greater than those previously described. These results show the need for a reevaluation of both the upper limit of cortical reorganization in adult primates and the mechanisms responsible for it.

Retinal cells have been induced to project into the medial geniculate nucleus, the principal auditory thalamic nucleus, in newborn ferrets by reduction of targets of retinal axons in one hemisphere and creation of alternative terminal space for these fibers in the auditory thalamus. Many cells in the medial geniculate nucleus are then visually driven, have large receptive fields, and receive input from retinal ganglion cells with small somata and slow conduction velocities. Visual cells with long conduction latencies and large contralateral receptive fields can also be recorded in primary auditory cortex. Some visual cells in auditory cortex are direction selective or have oriented receptive fields that resemble those of complex cells in primary visual cortex. Thus, functional visual projections can be routed into nonvisual structures in higher mammals, suggesting that the modality of a sensory thalamic nucleus or cortical area …

Microelectrode recordings were used to investigate the tonotopic organization of auditory cortex of macaque monkeys and guide the placement of injections of wheat germ agglutininhorse radish peroxidase (WGA‐HRP) and fluorescent dyes. Anatomical and physiological results were later related to histological distinctions in the same brains after sections were processed for cytoarchitecture, myeloarchitecture, acetylcholinesterase (AchE), or cytochrome oxidase (CO). The experiments produced serveral major findings. (1) Neurons throughout a broad expanse of cortex were highly responsive to pure tones, and best frequencies could be determined for neurons in arrays of recording sites. (2) The microelectrode recordings revealed two systematic representations of tone frequencies, the primary area (AI) and a primary‐like rostral field (R) as previously described. The representation of high to low frequency tones …

Removal of the representation of a specific body part in the postcentral cortex of the macaque resulted in the somatic deactivation of the corresponding body part in the second somatosensory area. In contrast, removal of the entire second somatosensory area had no grossly detectable effect on the somatic responsivity of neurons in the postcentral cortex. This direct electrophysiological evidence for serial cortical processing in somesthesia is similar to that found earlier for vision and, taken together with recent anatomical evidence, suggests that there is a common cortical plan for the processing of sensory information in the various sensory modalities.

Area 2 is a traditional architectonic subdivision of anterior parietal cortex in macaque monkeys, but its overall somatotopic organization and responsiveness to different types of somatic stimuli are poorly understood, and there are uncertainties concerning its rostral and caudal extent. The goals of the present study were to define the rostral and caudal borders of area 2 better, and to describe its overall organization and responsiveness. Somatic receptive fields were defined for hundreds of closely spaced microelectrode recording sites in postcentral parietal cortex of individual macaque monkeys anesthetized with ketamine. Electrophysiological and architectonic evidence suggested that a 3–4‐mm‐wide strip of cortex along the caudal border of area 1 includes all or most of area 2. The most lateral explored portion of area 2 adjoined the representation of the face in area 1. Much of this sector of area 2 was activated …

1. Selective ablations of the hand representations in postcentral cortical areas 3a, 3b, 1, and 2 were made in different combinations to determine each area's contribution to the responsivity and modality properties of neurons in the hand representation in SII. 2. Ablations that left intact only the postcentral areas that process predominantly cutaneous inputs (i.e., areas 3b and 1) yielded SII recording sites responsive to cutaneous stimulation and none driven exclusively by high-intensity or "deep" stimulation. Conversely, ablations that left intact only the postcentral areas that process predominantly deep receptor inputs (i.e., areas 3a and 2) yielded mostly SII recording sites that responded exclusively to deep stimulation. 3. Ablations that left intact only area 3a or only area 2 yielded substantial and roughly equal reductions in the number of deep receptive fields in SII. By contrast, ablations that left intact only area 3b or …

Large changes in somatotopic organization can be induced in adult primate somatosensory cortex by cutting peripheral afferents. The role, if any, of the thalamus in these changes has not been investigated previously. In the present experiments, electrophysiological recording in the ventroposterior lateral nucleus (VPL) has revealed that not only can reorganization occur in the thalamus, but it may be as extensive as that revealed in the cortex of the same monkeys. Thus, for at least some types of deafferentation, the reorganization revealed in the cortex may depend largely on subcortical changes.

Tonotopic organization is an essential feature of the primary auditory area (A1) of primate cortex. ln A1 of macaque monkeys, low frequencies are represented rostrolaterally and high frequencies are represented caudomedially. The purpose of this study was to determine if changes occur in this tonotopic organization following cochlear hearing loss. Under anesthesia, the superior temporal gyrus of adult macaque monkeys was exposed, and the tonotopic organization of A1 was mapped using conventional microelectrode recording techniques. Following recovery, the monkeys were selectively deafened for high frequencies using kanamycin and furosemide. The actual frequencies deafened were determined by the loss of tone-burst elicited auditory brainstem responses. Three months after deafening, A1 was remapped. Postmortem cytoarchitectural features identifying A1 were correlated with the electrophysiologic …

When a portion of primary somatosensory cortex is deprived of its normal inputs by peripheral nerve transection, intact skin surfaces represented in surrounding cortex come to activate the deprived zone within 2 months. We found that this cortical reorganization was accompanied by a marked decrease in the antibody staining of γ-aminobutyric acid (GABA) within the deprived sector of cortex in monkeys surviving nerve injury for 2-5 months. In contrast, there were no apparent changes in cytochrome oxidase reactivity in the deprived cortex of these same monkeys. Reduced levels of inhibition could allow previously unexpressed connections to become potent. Thus, the regulation of the expression of GABA appears to be one mechanism for maintaining and altering cortical representations.

We have reported that elimination of the representation of any body part in the primary (i.e., postcentral) somatosensory cortex of the adult macaque selectively eliminates the representation of that same body part in the second somatosensory area SII. We now report that, although removal of the entire postcentral hand representation does indeed leave the SII hand representation unresponsive to somatic stimulation initially, 6-8 weeks later this cortex is no longer silent. Instead, most or all of the region that had been vacated by the hand representation is now found to be occupied by an expanded foot representation. This massive somatotopic reorganization, involving more than half the areal extent of SII, exceeds that previously observed in the postcentral cortex after peripheral nerve damage and may reflect a greater capacity for reorganizational changes in higher order than in primary sensory cortical areas.

In adult monkeys, peripheral nerve injuries induce dramatic examples of neural plasticity in somatosensory cortex. It has been suggested that a cortical distance limit exists and that the amount of plasticity that is possible after injury is constrained by this limit. We have investigated this possibility by depriving a relatively large expanse of cortex by transecting and ligating both the median and the ulnar nerves to the hand. Electrophysiological recording in cortical areas 3b and 1 in three adult squirrel monkeys no less than 2 months after nerve transection has revealed that cutaneous responsiveness is regained throughout the deprived cortex and that a roughly normal topographic order is reestablished for the reorganized cortex.

Topographic maps in adult primate somatosensory cortex are capable of dramatic reorganizations after peripheral nerve injuries. In the present experiments, we have deprived a circumscribed portion of the hand map in somatosensory cortex of four adult squirrel monkeys by transecting the median nerve to one hand, and evaluated the hypothesis that N‐methyl‐d‐aspartate (NMDA) glutamatergic receptors are necessary for the reorganization that follows within four weeks. In one monkey, we confirm previous results demonstrating that the deprived cortex has regained responsiveness in its expanse four weeks after median nerve transection. However, in three monkeys in which NMDA receptors were concurrently blocked, most of the deprived cortex remained unresponsive. Thus, much of the cortical “recovery” that typically follows peripheral nerve injury in adult monkeys is apparently dependent on NMDA …

Cortex traditionally referred to as S-I in monkeys is a composite of 4 separate and complete representations of the contralateral body surface, one in each of the 4 cytoarchitectonic fields, areas 3a, 3b, 1, and 2. We investigated the significance of interconnections between these architectonic areas by assessing the immediate effects of ablations of parts of areas 3a and 3b on the responsivity of neurons in area 1. Ablations of specific parts of the hand representations in areas 3a and 3b immediately deactivated the corresponding part of the hand representation in area 1. We conclude that the processing of somesthetic inputs across anterior parietal cortex is predominantly hierarchical.

We have studied the morphology of single thalamocortical axons innervating area 3b of postcentral somatosensory cortex in macaque monkeys. We recorded from axons in the white matter below the representation of the hand in postcentral cortex in two monkeys (Macaca fascicularis) by using micropipettes filled with horseradish peroxidase (HRP). When an axon was recorded, we delineated its receptive field and determined its modality, and if cutaneous, whether it was slowly or rapidly adapting (SA or RA). We then impaled the axon and injected it with HRP. We recorded and successfully injected many more RA than SA axons, possibly because of differences in their true proportions. The RA axonal arbors varied in mediolateral extent from 350 to 800 μ with a mean of 600 μ One of the RA axons gave rise to four separate arbors spanning 2.5‐3.0 mm of cortex. The single SA axon we recovered was 370 μ in width …

Multiunit microelectrode recordings were used to explore the responsiveness and somatotopic organization of the representation of the hand in area 3b of anesthetized macaque monkeys. Major findings were as follows: (1) Recording sites throughout the hand representation were activated by low-threshold cutaneous stimulation. (2) Simple, punctate mechanical stimuli were highly effective in activating neurons. Neurons had small, restricted receptive fields. (3) Representations of nearly all skin surfaces of the hand were demonstrated in individual monkeys. (4) The basic topographic pattern found in all monkeys included the following: (a) a large sequential representation of the glabrous digits from thumb to little finger from lateral to medial in cortex, and from proximal to distal hand parts in cortex extending down the caudal bank of the central sulcus; (b) moderately large representations of radial and ulnar pads of …