P. E. Garraghty

Functional reorganization in adult monkey thalamus after peripheral nerve injury.

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.

Injury-induced reorganization of somatosensory cortex is accompanied by reductions in GABA staining.

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 gamma-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.

Ablations of Areas 3b (SI Proper) and 3a of Somatosensory Cortex in Marmosets Deactivate the Second and Parietal Ventral Somatosensory Areas

Partial ablations of specific parts of cortical areas 3b (SI proper) and 3a in marmosets were found to render somatotopically equivalent parts of two other cortical somatosensory fields, the second somatosensory area (SII) and the parietal ventral area (PV), unresponsive to peripheral stimulation. Microelectrode recordings in anesthetized marmosets first established the responsiveness and locations of the representations of body parts, including the hand in areas 3a and 3b, SII, and in some cases PV. The hand representations in areas 3a and 3b were then removed by aspiration. Immediately afterwards, additional recordings established that regions of SII and PV that formerly represented the hand were no longer responsive to cutaneous stimulation of the hand (or any other skin surface). Other parts of these fields, representing parts of the body other than the hand, remained responsive to stimulation of the previously effective receptive fields. We conclude that SII and PV depend on inputs (either direct or indirect) from areas 3a and 3b for their activation.

Ablations of areas 3a and 3b of monkey somatosensory cortex abolish cutaneous responsivity in area 1.

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.

Pattern of Peripheral Deafferentation Predicts Reorganizational Limits in Adult Primate Somatosensory Cortex

Previous experiments have shown that the reorganization of the hand representations in areas 3b and 1 of somatosensory cortex of monkeys can be extensive or limited, depending on the pattern of peripheral sensory loss. After the loss of two or more digits, the deprived zones of cortex are not fully reactivated by remaining inputs from the hand (Merzenich et al., 1984). In contrast, after deafferentation of the entire glabrous surface of the hand, the deprived cortex becomes responsive throughout its extent to cutaneous stimulation of the dorsal hairy surface of the hand (Garraghty and Kaas, 1991). To test the hypothesis that it is the pattern of sensory loss and not the deprivation procedure that results in these differences, we mimicked multiple-digit amputation by deafferenting corresponding parts of the dorsal and ventral hand. We then recorded from areas 3b and 1 of 3 squirrel monkeys 3-11 months after the deafferentation. In each case, much of the cortex normally activated by the removed inputs remained unresponsive to cutaneous stimulation of skin surfaces of the hand with intact innervation. Thus, the reorganization that can occur in somatosensory cortex following peripheral sensory loss is constrained by the precise content of the stimulus deprivation; that is, there is a limit to the set of new receptive fields cortical neurons can acquire.

Dynamic features of sensory and motor maps

Abstract Recent data support the idea that the functional organizations of sensory and motor maps in the mature brain are dynamically maintained. Experiments employing peripheral injuries or other manipulations indicate that these maps are capable of extensive reorganization. A number of candidate mechanisms for these changes have been suggested, providing avenues for further research.

The arbors of axons terminating in middle cortical layers of somatosensory area 3b in owl monkeys.

The arbors of single axons terminating predominantly in layer IV of the representation of the hand in area 3b of owl monkeys were reconstructed from serial brain sections after axons beneath the cortex were severed and horseradish peroxidase was injected into the white matter. In addition to dense terminations in layer IV, these labeled axons generally had branches extending into deeper layer III, and a few had very sparse terminations in layer VI. Terminal arbors ranged from 100 to 900 microns in diameter, and fine branches with synaptic boutons were unevenly distributed, typically grouped in a large central cluster and one or more smaller side clusters. The results are consistent with three broad conclusions: (1) Since the arbors are large relative to the details of the somatotopic map in area 3b, all regions within a single arbor may not be equally effective in activating cortical cells. (2) Spatially separate branches of single axons may relate to spatially separate modules of neurons of the same class in a manner that allows them to receive the same inputs. (3) Many of the somatotopic changes that have been reported in the hand representation as a result of nerve manipulations in adults could result from alterations in synaptic effectiveness within the arbors of single axons.

A sequential representation of the occiput, arm, forearm and hand across the rostrocaudal dimension of areas 1, 2 and 5 in macaque monkeys

Receptive fields were determined for recording sites in cortical areas 1, 2 and 5 in macaque monkeys. While a mixture of cutaneous and deep receptors were represented in most regions of area 2, a specific mediolateral level of area 2 was highly responsive to cutaneous input. Anteroposterior rows of recording sites across areas 1, 2 and 5 at this mediolateral location revealed a continuous sequence of cutaneous receptive fields proceeding from the occiput and face in area 1 to the forearm and hand in area 5.

Sprouting of peripheral nerve axons in the spinal cord of monkeys

It has been previously suggested that two conditions must be met in order for sprouting to occur in the dorsal horn of the spinal cord: afferent fibers must be stimulated to grow and alternate synaptic sites must be made available. We show that reversibly deactivating peripheral nerve axons by nerve crush alone, which produces little or no additional available synaptic sites, results in expansion of the peripheral nerve inputs in the spinal cord in both adult and infant macaque monkeys.

Hierarchical, parallel, and serial arrangements of sensory cortical areas: connection patterns and functional aspects

Recent studies have led to a better understanding of the organization and connections of somatosensory and visual cortex in a number of mammalian species. Lesion studies have provided information on the significance of particular connections. The variable effectiveness of cortical lesions in deactivating target areas suggests that serial processing may be emphasized in higher primates.