Reorganization of somatosensory area 3b representations in adult owl monkeys after digital syndactyly

1991 ◽  
Vol 66 (3) ◽  
pp. 1048-1058 ◽  
Author(s):  
T. Allard ◽  
S. A. Clark ◽  
W. M. Jenkins ◽  
M. M. Merzenich
Keyword(s):  
Temporal Structure ◽  
Receptive Fields ◽  
Somatosensory System ◽  
Critical Time ◽  
Experimental Manipulation ◽  
Afferent Input ◽  
Single Digit ◽  
Cortical Maps ◽  
Afferent Inputs ◽  
Area 3B

1. These experiments were designed to test the hypothesis that temporally correlated afferent input activity plays a lifelong role in the establishment and modification of receptive fields (RFs) and representational topographies in the primary somatosensory cortex of adult monkeys. They were based in part on the finding that adjacent digits of the hand are represented discontinuously in area 3b of the adult owl monkey. If cortical receptive fields and the details of cortical topographic representations are shaped by the weights of the temporal correlations among afferent inputs, then representational discontinuities between digits would be expected to arise because inputs from the skin surfaces of adjacent digits are largely independent in the critical time domain. 2. In the present experiments, the skin of adjacent digits 3 and 4 of the monkey hand was surgically connected to create an artificial syndactyly, or webbed-finger condition. Highly detailed microelectrode maps of the cortical representation of the syndactyl digits were obtained 3-7.5 mo later. This experimental manipulation greatly increased the amount of simultaneous or nearly simultaneous input from the normally separated, now fused, surfaces of adjacent fingers. 3. Cortical maps of the representations of finger surfaces were highly modified from the normal after a several-month-long period of digital fusion. Specifically, the normal discontinuity between the cortical representations of adjacent fingers was abolished. Within a wide cortical zone, RFs were defined that extended across the line of syndactyly onto the surgically joined skin of both fused digits. The representational topography of the fused digits was similar to any normal single digit and was characterized by a continuous progression of partially overlapping RFs. 4. Control observations revealed that these reorganizational changes cannot be accounted for by any changes in cutaneous innervation induced by the surgery. They must arise from representational changes in the central somatosensory system. 5. These findings reveal that cortical maps can be altered in detail in adult monkeys by modifying the distributed temporal structure of afferent inputs. They support the longstanding hypothesis that the temporal coincidence of inputs plays a role in the grouping of input subsets into specific cortical RFs and, consequently, in the shaping of selected effective cortical inputs and representational topographies throughout life.

Serial and parallel processing of tactual information in somatosensory cortex of rhesus monkeys

1992 ◽  
Vol 68 (2) ◽  
pp. 518-527 ◽  
Author(s):  
T. P. Pons ◽  
P. E. Garraghty ◽  
M. Mishkin
Keyword(s):  
Substantial Reduction ◽  
Receptive Fields ◽  
Somatosensory System ◽  
Encounter Rate ◽  
Specific Information ◽  
Tactile Information ◽  
Cortical Areas ◽  
Area 3A ◽  
Area 3B ◽  
Made In

1. Selective ablations of the hand representations in postcentral cortical areas 3a, 3b, 1, and 2 were made in different combinations to determine each area's contribution to the responsivity and modality properties of neurons in the hand representation in SII. 2. Ablations that left intact only the postcentral areas that process predominantly cutaneous inputs (i.e., areas 3b and 1) yielded SII recording sites responsive to cutaneous stimulation and none driven exclusively by high-intensity or "deep" stimulation. Conversely, ablations that left intact only the postcentral areas that process predominantly deep receptor inputs (i.e., areas 3a and 2) yielded mostly SII recording sites that responded exclusively to deep stimulation. 3. Ablations that left intact only area 3a or only area 2 yielded substantial and roughly equal reductions in the number of deep receptive fields in SII. By contrast, ablations that left intact only area 3b or only area 1 yielded unequal reductions in the number of cutaneous receptive fields in SII: a small reduction when area 3b alone was intact but a somewhat larger one when only area 1 was intact. 4. Finally, when the hand representation in area 3b was ablated, leaving areas 3a, 1, and 2 fully intact, there was again a substantial reduction in the encounter rate of cutaneous receptive fields. 5. The partial ablations often led to unresponsive sites in the SII hand representation. In SII representations other than of the hand no such unresponsive sites were found and there were no substantial changes in the ratio of cutaneous to deep receptive fields, indicating that the foregoing results were not due to long-lasting postsurgical depression or effects of anesthesia. 6. The findings indicate that modality-specific information is relayed from postcentral cortical areas to SII along parallel channels, with cutaneous inputs transmitted via areas 3b and 1, and deep inputs via areas 3a and 2. Further, area 3b provides the major source of cutaneous input to SII, directly and perhaps also via area 1. 7. The results are in line with accumulating anatomic and electrophysiologic evidence pointing to an evolutionary shift in the organization of the somatosensory system from the general mammalian plan, in which tactile information is processed in parallel in SI and SII, to a new organization in higher primates in which the processing of tactile information proceeds serially from SI to SII. The presumed functional advantages of this evolutionary shift are unknown.

Modular distribution of neurons with slowly adapting and rapidly adapting responses in area 3b of somatosensory cortex in monkeys

1984 ◽  
Vol 51 (4) ◽  
pp. 724-744 ◽  
Author(s):  
M. Sur ◽  
J. T. Wall ◽  
J. H. Kaas
Keyword(s):  
Somatosensory Cortex ◽  
Receptive Fields ◽  
Systematic Position ◽  
Stimulus Onset ◽  
Cortical Layers ◽  
Single Digit ◽  
Macaque Monkeys ◽  
Predominant Orientation ◽  
Skin Indentation ◽  
Area 3B

Recordings from the representations of the glabrous digits in area 3b of the somatosensory cortex of owl and macaque monkeys revealed two types of neurons. Rapidly adapting (RA) neurons responded only at the onset and offset of a 1-s skin indentation. Slowly adapting (SA) neurons also responded to stimulus onset and offset but, in addition, they responded throughout the 1-s skin indentation. RA neurons were found in all cortical layers while SA neurons were found only in the middle cortical layers. In electrode penetrations perpendicular to the layers, some penetrations encountered only RA neurons (RA penetrations), while other penetrations first encountered RA neurons, then SA neurons, and finally RA neurons again (SA penetrations). When closely spaced electrode penetrations were made throughout the representation of a single digit, it was apparent that RA and SA penetrations were not randomly distributed. The distribution suggested the existence of separate clusters or bands of SA and RA neurons in the middle layers of cortex. The predominant orientation of the SA and RA regions was rostrocaudally along the lengths of the digit representations. The SA and RA bands varied in width, had no systematic position in the representation of individual digits, and often crossed from the representation of one digit to another. Because of overlapping receptive fields for neurons in adjoining bands, the SA and RA bands appeared to represent the digits separately. This would allow all skin surfaces for each digit to be subserved by both types of neurons.

scholarly journals A neural surveyor in somatosensory cortex

2020 ◽  
Author(s):  
Luke E. Miller ◽  
Cécile Fabio ◽  
Rob van Beers ◽  
Alessandro Farnè ◽  
W. Pieter Medendorp
Keyword(s):  
Somatosensory Cortex ◽  
Somatosensory System ◽  
Afferent Input ◽  
Feedforward Neural Network ◽  
The Body ◽  
Tuning Curves ◽  
Tactile Localization ◽  
Neural Signature ◽  
Sensory Map ◽  
Area 3B

SummaryPerhaps the most recognizable sensory map in all of neuroscience is the somatosensory homunculus. Though it seems straightforward, this simple representation belies the complex link between an activation in somatosensory Area 3b and the associated touch location on the body. Any isolated activation is spatially ambiguous without a neural decoder that can read its position within the entire map, though how this is computed by neural networks is unknown. We propose that somatosensory cortex implements multilateration, a common computation used by surveying and GPS systems to localize objects. Specifically, to decode touch location on the body, the somatosensory system estimates the relative distance between the afferent input and the body’s joints. We show that a simple feedforward neural network which captures the receptive field properties of somatosensory cortex implements a Bayes-optimal multilateral decoder via a combination of bell-shaped (Area 3b) and sigmoidal (Areas 1/2) tuning curves. Simulations demonstrated that this decoder produced a unique pattern of localization variability between two joints that was not produced by other known neural decoders. Finally, we identify this neural signature of multilateration in actual psychophysical experiments, suggesting that it is a candidate computational mechanism underlying tactile localization.

Receptive-field changes induced by peripheral nerve stimulation in SI of adult cats

1990 ◽  
Vol 63 (5) ◽  
pp. 1213-1225 ◽  
Author(s):  
G. H. Recanzone ◽  
T. T. Allard ◽  
W. M. Jenkins ◽  
M. M. Merzenich
Keyword(s):  
Nerve Stimulation ◽  
Large Diameter ◽  
Receptive Fields ◽  
Somatosensory System ◽  
Opiate Antagonist ◽  
Stimulation Period ◽  
Afferent Inputs ◽  
Adult Cats ◽  
Induced Changes ◽  
Stimulation Control

1. Receptive fields (RFs) of neurons in the primary somatosensory (SI) cortex were defined before, during, and after electrical stimulation of myelinated fibers in the dorsal cutaneous branch of the ulnar nerve in adult pentobarbital sodium-anesthetized cats. 2. This stimulation resulted in an approximately threefold increase of SI multiunit RF sizes. Substantial changes were first recorded within 1-2 h of stimulation. RFs typically enlarged continuously over a several-hour stimulation period, then stabilized. 3. RF-area increases were observed within both the forepaw and hindpaw representational zones in the SI cortex contralateral to the stimulated forepaw nerve. RF sizes did not increase in the ipsilateral SI body surface representation or in sham-stimulation control animals. 4. Preliminary studies indicate that stimulation-induced changes can be halted and often reversed by the intravenous administration of the opiate antagonist naloxone. 5. These observations suggest a global naloxone-sensitive modulatory system that operates on large-diameter afferent inputs in the cat somatosensory system. The increases in RF size occur under nerve-stimulation conditions similar to those that result in the generation of widespread analgesia (Chung et al. 1984a,b; Gamble and Milne 1986; Toda and Ichioka 1978).

scholarly journals Response Properties of Neurons in Primary Somatosensory Cortex of Owl Monkeys Reflect Widespread Spatiotemporal Integration

2010 ◽  
Vol 103 (4) ◽  
pp. 2139-2157 ◽  
Author(s):  
Jamie L. Reed ◽  
Hui-Xin Qi ◽  
Zhiyi Zhou ◽  
Melanie R. Bernard ◽  
Mark J. Burish ◽  
...  
Keyword(s):  
Receptive Fields ◽  
Single Neurons ◽  
Electrode Arrays ◽  
Single Digit ◽  
Firing Rates ◽  
Paired Stimulation ◽  
The Mean ◽  
Owl Monkeys ◽  
Preferred Stimulus ◽  
Area 3B

Receptive fields of neurons in somatosensory area 3b of monkeys are typically described as restricted to part of a single digit or palm pad. However, such neurons are likely involved in integrating stimulus information from across the hand. To evaluate this possibility, we recorded from area 3b neurons in anesthetized owl monkeys with 100-electrode arrays, stimulating two hand locations with electromechanical probes simultaneously or asynchronously. Response magnitudes and latencies of single- and multiunits varied with stimulus conditions, and multiunit responses were similar to single-unit responses. The mean peak firing rate for single neurons stimulated within the preferred location was estimated to be ∼26 spike/s. Simultaneous stimulation with a second probe outside the preferred location slightly decreased peak firing rates to ∼22 spike/s. When the nonpreferred stimulus preceded the preferred stimulus by 10–500 ms, peak firing rates were suppressed with greatest suppression when the nonpreferred stimulus preceded by 30 ms (∼7 spike/s). The mean latency for single neurons stimulated within the preferred location was ∼23 ms, and latency was little affected by simultaneous paired stimulation. However, when the nonpreferred stimulus preceded the preferred stimulus by 10 ms, latencies shortened to ∼16 ms. Response suppression occurred even when stimuli were separated by long distances (nonadjacent digits) or long times (500 ms onset asynchrony). Facilitation, though rare, occurred most often when the stimulus onsets were within 0–30 ms of each other. These findings quantify spatiotemporal interactions and support the hypothesis that area 3b is involved in widespread stimulus integration.

scholarly journals Tactile orientation perception: an ideal observer analysis of human psychophysical performance in relation to macaque area 3b receptive fields

2015 ◽  
Vol 114 (6) ◽  
pp. 3076-3096 ◽  
Author(s):  
Ryan M. Peters ◽  
Phillip Staibano ◽  
Daniel Goldreich
Keyword(s):  
Cortical Neurons ◽  
Human Performance ◽  
Spatial Perception ◽  
Receptive Fields ◽  
Human Perception ◽  
Ideal Observer ◽  
Orientation Discrimination ◽  
Orientation Perception ◽  
Area 3B ◽  
The Ideal

The ability to resolve the orientation of edges is crucial to daily tactile and sensorimotor function, yet the means by which edge perception occurs is not well understood. Primate cortical area 3b neurons have diverse receptive field (RF) spatial structures that may participate in edge orientation perception. We evaluated five candidate RF models for macaque area 3b neurons, previously recorded while an oriented bar contacted the monkey's fingertip. We used a Bayesian classifier to assign each neuron a best-fit RF structure. We generated predictions for human performance by implementing an ideal observer that optimally decoded stimulus-evoked spike counts in the model neurons. The ideal observer predicted a saturating reduction in bar orientation discrimination threshold with increasing bar length. We tested 24 humans on an automated, precision-controlled bar orientation discrimination task and observed performance consistent with that predicted. We next queried the ideal observer to discover the RF structure and number of cortical neurons that best matched each participant's performance. Human perception was matched with a median of 24 model neurons firing throughout a 1-s period. The 10 lowest-performing participants were fit with RFs lacking inhibitory sidebands, whereas 12 of the 14 higher-performing participants were fit with RFs containing inhibitory sidebands. Participants whose discrimination improved as bar length increased to 10 mm were fit with longer RFs; those who performed well on the 2-mm bar, with narrower RFs. These results suggest plausible RF features and computational strategies underlying tactile spatial perception and may have implications for perceptual learning.

Interaction between chemoreceptor and stretch receptor inputs at medullary respiratory neurons

1994 ◽  
Vol 266 (6) ◽  
pp. R1951-R1961 ◽  
Author(s):  
J. Bajic ◽  
E. J. Zuperku ◽  
M. Tonkovic-Capin ◽  
F. A. Hopp
Keyword(s):  
Time Course ◽  
Afferent Input ◽  
Respiratory Neurons ◽  
Neuronal Responses ◽  
Additive Interaction ◽  
Dorsal Respiratory Group ◽  
Afferent Inputs ◽  
Discharge Patterns ◽  
Carotid Body Chemoreceptors ◽  
Common Carotid Arteries

The interaction between afferent inputs from carotid body chemoreceptors (CCRs) and from slowly adapting pulmonary stretch receptors (PSRs) on the discharge patterns of medullary inspiratory (I) and expiratory (E) neurons was characterized in thiopental sodium-anesthetized, paralyzed, ventilated dogs. A cycle-triggered ventilator was used to produce control and test pulmonary afferent input patterns. The CCRs were stimulated by phase-synchronized bolus injections of CO2-saturated saline into the common carotid arteries. Only those neurons whose discharge time course was altered by both inflation and CCR activation were studied. The dorsal respiratory group (DRG) I inflation-insensitive neurons were also included. Cycle-triggered histograms of unit activity were obtained for the neuronal responses to inflation, CO2 bolus, and their combination, as well as for the spontaneous control condition. Linearity of the interaction was tested by comparing the sum of the net individual responses to the net response of the combined afferent inputs. The results suggest that a linear (additive) interaction between CCR and PSR inputs exists for the DRG I inflation-sensitive neurons, the ventral respiratory group (VRG) I decrementing, and caudal VRG E augmenting neurons, while a nonadditive interaction exists for caudal VRG E decrementing bulbospinal neurons. The implications of these findings are discussed.

scholarly journals Relationship Between Physiological Response Type (RA and SA) and Vibrissal Receptive Field of Neurons Within the Rat Trigeminal Ganglion

2006 ◽  
Vol 95 (5) ◽  
pp. 3129-3145 ◽  
Author(s):  
Steven C. Leiser ◽  
Karen A. Moxon
Keyword(s):  
Trigeminal Ganglion ◽  
Three Dimensional ◽  
Receptive Fields ◽  
Somatosensory System ◽  
Response Type ◽  
Physiological Level ◽  
Somatotopic Organization ◽  
Tactile Stimuli ◽  
Distinct Features ◽  
The Relationship

Cells within the trigeminal ganglion (Vg) encode all the information necessary for the rat to differentiate tactile stimuli, yet it is the least-studied component in the rodent trigeminal somatosensory system. For example, extensive anatomical and electrophysiological investigations have shown clear somatotopic organization in the higher levels of this system, including VPM thalamus and SI cortex, yet whether this conserved schemata exists in the Vg is unknown. Moreover although there is recent interest in recording from vibrissae-responsive cells in the Vg, it is surprising to note that the locations of these cells have not even been clearly demarcated. To address this, we recorded extracellularly from 350 sensory-responsive Vg neurons in 35 Long-Evans rats. First, we determined three-dimensional locations of these cells and found a finer detail of somatotopy than previously reported. Cells innervating dorsal facial features, even within the whisker region, were more dorsal than midline and ventral features. We also show more cells with caudal than rostral whisker receptive fields (RF), similar to that found in VPM and SI. Next, for each vibrissal cell we determined its response type classified as either rapidly (RA) or slowly (SA) adapting. We examined the relationship between vibrissal RF and response type and demonstrate similar proportions of RA and SA cells responding to any whisker. These results suggest that if RA and SA cells encode distinct features of stimuli, as previously suggested, then at the basic physiological level each whisker has similar abilities to encode for such features.

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