Topology of the body representation in somatosensory area I of primates.
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Animals↗
Biomedical subjects
B L Whitsel
Publications and source records attributed to B L Whitsel.
Patterns of muscle spindle afferent stimulation by alkylammonium compounds.
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Animals↗
The topology of dermatomal projection in the medial lemniscal system.
1. The topographic organization of first order afferent fibres in the lumbar, sacral and coccygeal dorsal roots, and in the fasciculus gracilis was studied in squirrel monkeys.2. At the entry zone, progressing from caudal to rostral, dorsal root filaments receive fibres from tail and hind-limb receptive fields which serially overlap and describe a spiral-shaped trajectory. The latter starts with tail, progresses post-axially towards the foot, crosses the foot from lateral to medial, and ascends the preaxial leg.3. In the fasciculus gracilis, this arrangement of fibres at the dorsal root entry zone is preserved in its entirety. It assumes the form of a fibre lamination, with the most caudal dorsal root fibres occupying a dorso-medial location; further rostral dorsal root fibres come to lie more ventrolaterally.4. Dorsum and sole of foot project in an overlapping and interdigitating manner to the fibre lamina of the 7th lumber dermatome in the fasciculus gracilis. Thereby, dorsum and sole of foot behave in the projection as if they were one and the same surface.5. The argument is presented that the foot and its projection on to the cross-sectional plane of the dorsal funiculus are topologically equivalent and that the hind-limb as a whole and its projection are not. On the other hand, homotopic mapping of the foot together with the sequential fibre organization in the dorsal funiculus enable many more types of closed curves on the body surface to remain arc-wise connected in the projection than would otherwise be possible.
Animals↗
Organization of the vestibular projection to the spinal cord of the cat.
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Spatial organization of the peripheral input to area 1 cell columns. I. The detection of 'segregates'.
Extracellular single neuron recording methods are used to study the RFs of neurons comprising area 1 cell columns in unanesthetized Macaca fascicularis monkeys. The RF data obtained in approximately radial microelectrode penetrations demonstrate that the RFs of neurons located within the same area 1 cell columns can differ strikingly, and that it is common for neighboring neurons to possess RFs differing greatly in size or configuration. However, the RF variations detected within a typical area 1 cell mini-column (single cell radial column) appear to be substantially less than the variations observed for nearby neurons lying in different minicolumns. The RF data obtained from arrays of penetrations suggest that the skin representation in the forelimb region of area 1 is organized in a discontinuous, step-like fashion: as a mosaic of discrete 600 micron wide radial cell columns--segregates. Although the RFs of neurons of a segregate can vary substantially in size and configuration, they all share in common a single small area on the skin. The boundaries of a segregate can be mapped precisely because, unlike the situation for neurons located within the same segregate, some of the neurons located on opposite sides of a segregate boundary (belonging to different segregates) have non-overlapping RFs. Furthermore, it appears that within any given segregate there is no systematic shift in RF location as the electrode advances through a sequence of minicolumns. Systematic RF shifts occurred only when the electrode traversed the boundary between neighboring segregates.
Animals↗
Spatial organization of the peripheral input to area 1 cell columns. II. The forelimb representation achieved by a mosaic of segregates.
The view (advanced in the previous paper) that the topographic organization in the forelimb region of area 1 of Macaca fascicularis monkeys should be regarded as a mosaic of discrete units--segregates--is evaluated. It is found that in all cortical layers the RFs sampled within a single segregate possess a wide variety of sizes and configurations, and occupy a wide variety of positions on the skin relative to the segregate RF center (the latter is a small skin area common to RFs of all neurons in the segregate). This within-segregate RF variability is structured so that the position of RFs of neurons sampled from different sectors of a segregate exhibits little, if any, systematic shift. The skin area that provides sensory input to any given area 1 segregate (estimated by the aggregate of the RFs sampled from that segregate) is extensive. This 'segregate RF', however, is not homogenous: i.e. central regions of the segregate RF are included in the RFs of a higher fraction of the neurons in the segregate than are peripheral regions. Segregate RFs appear particularly extensive when their size is compared with a relatively small shift in skin position that takes place when one shifts from one segregate to the next. Consequently, the skin areas that provide the sensory inputs to neighboring segregates overlap to a very large degree; and even fairly remote segregates in area 1 can receive a substantial common input. The arrangement of segregate RFs in area 1 is, in general, somatotopic. Nevertheless, the local relationships that are obtained among different segregates can deviate significantly from a strictly somatotopic pattern. The area 1 topographic organization detected in this study appears to differ substantially from that described by other investigators. A more detailed analysis suggests that most of the major differences between this and the previous descriptions of area 1 organization may largely be attributable to the different experimental conditions employed, and that the results of this study and those described by workers using different mapping methods are, in fact, generally compatible. Finally, it is suggested that the mosaic pattern of the topographic organization detected in area 1 may reflect the bundled nature of its afferent input.
Animals↗
Mechanisms underlying somatosensory cortical dynamics: II. In vitro studies.
The response of the sensorimotor cortical slice to repetitive, single-site afferent drive is mapped using both evoked potential and metabolic mapping [2-deoxyglucose (2DG)] methods. Systematic changes (increases or decreases) in the evoked potential occur during repetitive 3-5 Hz stimulation. These resemble the changes in SI neuron response observed in the in vivo studies of the preceding companion article; they occur rapidly, recover within 1 min and are reproducible if stimulus parameters remain unchanged. Place, timing, and intensity of repetitive stimulation influence the amplitude and form of the response alterations observed at a given cortical locus. The neuron populations that exhibit different response modifications to the same repetitive stimulus are distributed nonrandomly in the slice: neurons occupying column-shaped aggregates undergo a common response alteration (either an increase or decrease) during repetitive stimulation, with sharp boundaries separating neighboring aggregates distinguishable on the basis of their dynamic behaviors. The distribution of stimulus-evoked 2DG uptake in the slice is "columnar," the dimensions of the 2DG columns corresponding to those mapped with neurophysiological methods. Taken together, the findings support the concept that repetitive stimulation causes the intrinsic network of somatosensory cortex to modify dynamically the network's response to extrinsic excitatory drive so that the local differences in the pattern of extrinsic excitatory drive to neighboring cortical columns are enhanced.
Afferent Pathways↗
Mechanisms underlying somatosensory cortical dynamics: I. In vivo studies.
The experiments of this study demonstrate that relatively modest rates of repetitive tactile stimulation are accompanied by rapid and reversible modifications (either increases or decreases) in the response of SI neurons. Complete recovery occurs in a few minutes following cessation of stimulation. The modifications are reproducible (1) if stimulus parameters remain the same and (2) if time for recovery is provided between successive exposures. In contrast, repetitive tactile stimuli identical to those that modify SI neuron response rarely lead to changes in the response of cutaneous mechanoreceptive afferents. SI neuron functional properties conventionally regarded as immutable [e.g., directional selectivity, and distribution of sensitivity within the receptive field (RF)] also modify with repetitive stimulation. While the changes in RF organization differ in detail from one neuron to the next, they are similar in form: the response generated by stimulus contact with one (or more rarely, several) RF region(s) becomes enhanced relative to the response the same stimulus evokes from neighboring regions. Neurons in the same column (sampled in the same radial penetration) exhibit very similar changes in the distribution of sensitivity within the RF, whereas neurons sampled in tangential penetrations exhibit diverse, apparently unrelated changes in RF organization in response to the same repetitive stimulus. Simultaneous multichannel recordings reveal that a repetitive tactile stimulus exerts similar effects on the response and RFs of the neurons within local (no more than 100 microns) neuron groupings. A model that incorporates a manner of SI topographical organization (segregate organization) and well-known aspects of neocortical cellular, neurotransmitter/receptor, and connectional architecture accounts for the changes in SI neuron behavior observed during repetitive stimulation.
Afferent Pathways↗
Minicolumnar activation patterns in cat and monkey SI cortex.
The distribution of stimulus-evoked 14C-2-deoxyglucose (2DG) labeling in primary somatosensory cortex (SI) of monkey (Macaca fascicularis) and cat was investigated. Reconstructions of the global pattern of labeling reveal that discrete skin stimuli evoke activity within an extensive region of SI, and that the activation pattern typically consists of multiple, elongated regions of above-background labeling ("modules," typically 0.5-1.0 mm wide, and 1-4 mm long). Evidence obtained using recently developed methods (Tommerdahl, 1989) for quantitative analysis of 2DG activity patterns is shown to be consistent with the idea (Whitsel et al., 1991) that SI modules typically are bounded by zones dominated by stimulus-evoked inhibition. The labeling pattern within individual 2DG modules in SI of both cats and monkeys is analyzed quantitatively (in the frequency domain). Within-module spatial activation patterns are demonstrated to be periodic, consisting of radially oriented profiles of above-background labeling separated from each other by less strongly labeled radial profiles. The spectral characteristics of within-module 2DG labeling change systematically with location along the module's long axis: spatial frequencies between 18 and 35 cycles/mm are prominent in the labeling that occupies both the middle and upper layers at central locations in the module, but are a less obvious component of the labeling in both the middle and upper layers at locations remote to the module center. Since the radially oriented periodic variation both (1) in 2DG labeling in regions of SI outside modules and (2) in optical density in images of Nissl-stained sections of SI consists predominantly of spatial frequencies in the range of 18-35 cycles/mm, it is concluded that the radial profiles of labeling within individual 2DG modules correspond to groupings of minicolumns distinguishable from their neighbors on the basis of labeling intensity. The findings raise the possibility that highly structured, within-module spatial patterns of SI minicolumnar activation encode information about the physical properties of tactile stimuli.
Animals↗
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
Acoustic Stimulation↗