Initial cortical reactions to injury of the median and radial nerves to the hands of adult primates.

The area 3b hand cortex of adult squirrel monkeys was mapped during the first minutes to hours after transecting the radial and median nerves to the hand. The objective was to evaluate initial cortical reactions to this injury and to determine whether patterns and extents of cortical change are similar in different individuals. There are 5 main findings. First, cortical aggregates related to ulnar nerve inputs from the hand rapidly expanded to occupy an additional 21% of the cortical hand map. Second, face and forearm inputs, which normally activate areas adjacent to hand cortex, rapidly expanded into areas of 4% and 1% of the hand cortex respectively. Third, cortical changes involved shifts in receptive field locations that were initiated within minutes after injury. Fourth, the spatial patterns and extents of cortical change were similar in different individuals. Finally, the pattern of cortical change produced after this injury differed from the pattern seen after injury of the median and ulnar nerves. These rapid expansions are a beginning point from which further changes must progress; however, in contrast to changes accompanying chronic hand injuries, these initial cortical reactions do not appear dictated by use of uninjured inputs.

The consistency, extent, and locations of early-onset changes in cortical nerve dominance aggregates following injury of nerves to primate hands.

The somatosensory cortex of primates contains patch- and bandlike aggregates of neurons that are dominantly activated by cutaneous inputs from the radial, median, and ulnar nerves to the hand. In the present study, the area 3b hand cortex of adult monkeys was mapped immediately before and after combined median and ulnar nerve transection to evaluate the consistency, extent, and location of early post-injury alterations in the deprived median and ulnar nerve cortical bands. Several alterations were observed acutely after injury. (1) The patchlike cortical aggregates of intact radial nerve inputs from the hand underwent a two- to three-fold expansion. This expansion was not related to peripheral changes in the radial nerve skin territory, but was due to rapid central decompression of radial nerve dominance patches. (2) The largest changes involved patches in lateral to central locations of the hand map. (3) The expanded patches occupied cortical zones that were activated by inputs from the digits, palm, and posterior hand prior to injury. These receptive field shifts were initiated within minutes after injury. (4) Receptive fields of neurons within expanded radial nerve patches were normal in size. (5) Besides changes involving radial nerve inputs from the hand, there was a small expansion of forelimb inputs into the preinjury hand cortex; however, the representation of face inputs did not expand into this cortex. (6) Finally, neurons across 50-69% of the hand cortex were unresponsive to tactile stimuli acutely after this injury. These findings indicate that the distribution patterns of nerve dominance aggregates in adult primates begin changing within minutes after nerve injury. Cortical changes involving specific inputs occupy similar extents and locations of cortex, and are arranged in highly consistent patterns, in different individuals. It is suggested that this consistency reflects specific patterns of central sensitization or disinhibition that are triggered by the injury.

Nerve innervation of the hand and associated nerve dominance aggregates in the somatosensory cortex of a primate (squirrel monkey).

The cutaneous innervation territories of the median, ulnar, and radial nerves to the hand were determined from neurophysiological recordings of peripheral mechanoreceptor axons in adult squirrel monkeys. These territories were then related to cutaneous receptive fields of cortical area 3b neurons to determine how low-threshold inputs from each hand nerve map onto the primary somatosensory cortex. The results indicate that mechanoreceptor axons in each nerve innervate a continuous skin territory covering about 40% of the hand surface. The total territory of each nerve contains subregions of skin that are either autonomously innervated by that nerve or that receive overlapping innervation from more than one nerve. The autonomous, overlap, and total territories of each nerve are relatively constant from hand to hand. In the area 3b cortex, low-threshold afferents from each nerve provide inputs to aggregates of cortical neurons. The cortical aggregates relating to the median and ulnar nerves are arranged as continuous, rostrocaudally oriented bands, whereas aggregates relating to the radial nerve are discontinuous and more patch-like. Similar patterns of bands and patches, and similar compression ratios of skin/cortical area, are seen across different monkeys. These findings demonstrate that the primary somatosensory cortex of normal adult primates contains bands or patches of neurons that are dominantly activated by low-threshold inputs from specific hand nerves. This approach of delineating nerve territories and their related cortical dominance aggregates provides a useful means of analyzing cortical images of nerves and of quantitating peripheral and central patterns of deprivation after nerve injury.

Current hypotheses of structural pattern formation in the somatosensory system and their potential relevance to humans.

Current hypotheses of structural pattern formation in the mammalian somatosensory system are modeled on experimental findings from the trigeminal system of rodents. The present results show that, like rodents, the trigeminal nucleus principalis of humans contains a parcellated pattern of cytochrome oxidase dense patches. These results provide an indication of the potential usefulness of rodent-based hypotheses for understanding pattern formation in human somatosensory connections.