EFFECTS OF SPINAL DORSAL COLUMN TRANSECTION ON THE RESPONSE OF MONKEYANTERIOR PARIETAL CORTEX TO REPETITIVE SKIN STIMULATION

The pattern of C-14-2-deoxyglucose (2DG) labeling in anterior parietal cortex was evaluated in three groups of experimental subjects: (1) su bjects in which all spinal pathways projecting at short latency to the contralateral hemisphere were intact, (2) subjects with either unilat eral or bilateral transection of the dorsal column pathway, and (3) su bjects in whom a two-stage tractotomy (dorsal column isolation) restri cted short-latency mechanoreceptor drive to that conveyed via the dors al column pathway, Macaca fascicularis and Macaca arctoides monkeys we re studied. When the spinal cord pathways projecting at short latency to contralateral anterior parietal cortex were intact, controlled vibr otactile or skin brushing stimuli evoked one or, more rarely, several loci of maximal 20G uptake (typically 1.5-2.5 mm in diameter) in the t opographically appropriate location(s) within area 3b and/or area 1. T he labeling at each locus of maximal 2DG uptake extended continuously across layers Il-VI. Each locus of maximal 200 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 3 a, and/or from area 1 into area 2. In the absence of skin stimulation, little or no above-background 200 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 comple te transection of the spinal dorsal column the global 200 pattern evok ed by a repetitive skin stimulus in contralateral anterior parietal co rtex was a near mirror image of the pattern evoked by the same stimulu s in intact subjects. In the absence of the dorsal column path, neithe r 10-25 Hz vibrotactile nor brushing stimulation evoked above-backgrou nd uptake at the topographically appropriate location(s) within contra lateral area 35 and/or area 1. Instead, a prominent region of below-ba ckground 200 uptake occupied the topographically appropriate location in area 3b and/or area 1, and the region of suppressed 200 uptake was bounded by one or more regions of above-background 200 uptake that ext ended from areas 35 or 1 into area 3a and/or into area 2. When a two-s tage spinal tractotomy prevented stimulus-evoked short-latency input f rom reaching contralateral anterior parietal cortex via pathways other than the dorsal column, the 200 activity patterns evoked in contralat eral 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 devel oped to evaluate the hypothesis that the observed conical effects of d orsal column transection might be attributable, at least in part, to i nhibitory interactions among anterior parietal cortical regions that r eceive their principal input from different spinal cord pathways. The model incorporated known features of (1) the conical projection of spi nal somatosensory pathways, (2) anterior parietal intrinsic and long-d istance horizontal connectivity, and (3) certain neurotransmitter/rece ptor systems characteristic of sensory neocortex. Simulations of the m odel network provided results consistent with the idea that repetitive skin stimuli evoke maladaptive, time-dependent corticocortical intera ctions within anterior parietal cortex contralateral to a dorsal colum n 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 upt ake 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 ct al., 197 4; Vierck et al., 1990a; Makous and Vierck, 1994), and (3) abnormal ti me-dependent characteristics of tactile perception in monkeys with dor sal column lesions (Vierck, 1973; Vierck et al., 1983, 1985, 1990b).