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Effects of spinal dorsal column transection on the response of monkey anterior parietal cortex to repetitive skin stimulation.

The pattern of 14C-2-deoxyglucose (2DG) labeling in anterior parietal cortex was evaluated in three groups of experimental subjects: (1) subjects in which all spinal pathways projecting at short latency to the contralateral hemisphere were intact, (2) subjects with either unilateral or bilateral transection of the dorsal column pathway, and (3) subjects in whom a two-stage tractotomy (dorsal column isolation) restricted short-latency mechanoreceptor drive to that conveyed via the dorsal column pathway. Macaca fascicularis and Macaca arctoides monkeys were studied. When the spinal cord pathways projecting at short latency to contralateral anterior parietal cortex were intact, controlled vibrotactile or skin brushing stimuli evoked one or, more rarely, several loci of maximal 2DG uptake (typically 1.5-2.5 mm in diameter) in the topographically appropriate location(s) within area 3b and/or area 1. The labeling at each locus of maximal 2DG uptake extended continuously across layers II-VI. Each locus of maximal 2DG uptake was bordered on one or more sides by irregularly shaped zones of below-background 2DG uptake that could extend without interruption from area 3b into area 3a, and/or from area 1 into area 2. In the absence of skin stimulation, little or no above-background 2DG uptake occurred at any locus within areas 3b and 1 of subjects in which the dorsal column pathway on the opposite side of the spinal cord was intact. In subjects with a complete transection of the spinal dorsal column the global 2DG pattern evoked by a repetitive skin stimulus in contralateral anterior parietal cortex was a near mirror image of the pattern evoked by the same stimulus in intact subjects. In the absence of the dorsal column path, neither 10-25 Hz vibrotactile nor brushing stimulation evoked above-background uptake at the topographically appropriate location(s) within contralateral area 3b and/or area 1. Instead, a prominent region of below-background 2DG uptake occupied the topographically appropriate location in area 3b and/or area 1, and the region of suppressed 2DG uptake was bounded by one or more regions of above-background 2DG uptake that extended from areas 3b or 1 into area 3a and/or into area 2. When a two-stage spinal tractotomy prevented stimulus-evoked short-latency input from reaching contralateral anterior parietal cortex via pathways other than the dorsal column, the 2DG activity patterns evoked in contralateral cortex by either brushing or vibrotactile stimuli were similar to the patterns obtained when the somatosensory pathways on the opposite side of the spinal cord were intact. A neural network model was developed to evaluate the hypothesis that the observed cortical effects of dorsal column transection might be attributable, at least in part, to inhibitory interactions among anterior parietal cortical regions that receive their principal input from different spinal cord pathways. The model incorporated known features of (1) the cortical projection of spinal somatosensory pathways, (2) anterior parietal intrinsic and long-distance horizontal connectivity, and (3) certain neurotransmitter/receptor systems characteristic of sensory neocortex. Simulations of the model network provided results consistent with the idea that repetitive skin stimuli evoke maladaptive, time-dependent corticocortical interactions within anterior parietal cortex contralateral to a dorsal column lesion. The observations indicate that corticocortical interactions account for the (1) near mirror-image pattern (relative to the normal Mexican hat-like pattern) of anterior parietal stimulus-evoked 2DG uptake observed in subjects with a dorsal column lesion, (2) unusual time-dependent response properties of individual area 3b and 1 neurons or neuron populations deprived of dorsal column input (Dreyer et al., 1974; Vierck et al., 1990a; Makous and Vierck, 1994), and (3) abnormal time-dependent characteristics of tactile perception in monkeys with dorsal colum