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.

Transient and prolonged effects of acetylcholine on responsiveness of cat somatosensory cortical neurons

1988 ◽  
Vol 59 (4) ◽  
pp. 1253-1276 ◽  
Author(s):  
R. Metherate ◽  
N. Tremblay ◽  
R. W. Dykes
Keyword(s):  
Receptive Field ◽  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Receptive Fields ◽  
Fixed Dose ◽  
Cortical Layers ◽  
Afferent Inputs ◽  
Time Periods ◽  
Layer I ◽  
Layer Vi

1. Two-hundred and seven neurons were examined for changes in their responsiveness during the iontophoretic administration of acetylcholine (ACh) in barbiturate-anesthetized cats. 2. The laminar locations of 78 cells were determined. Cholinoceptive neurons were found in all cortical layers and ranged from 50% of the cells tested in layer I to 78% in layer VI. 3. When the responsiveness of a neuron was measured by the magnitude of the discharge generated by a fixed dose of glutamate, 30 of 47 cases (64%) were potentiated, and 4 (8%) were depressed when ACh was administered during glutamate-induced excitation. 4. ACh administered during glutamate excitation was significantly more effective in altering neuronal responsiveness than was ACh administered alone (P less than 0.001). 5. When the responsiveness of a neuron was measured by the magnitude of the discharge generated by a standard somatic stimulus applied to the receptive field, 42 of 52 cases (81%) were potentiated during ACh application. This was again different from ACh treatment alone where only 4 of 27 tests (15%) resulted in subsequent enhancement of the response to somatic stimuli. 6. ACh generally increased the responsiveness of neurons with peripheral receptive fields and caused the appearance of a receptive field in some cells lacking one. 7. In many cases the changes in excitability, as measured by responses either to glutamate or to somatic stimulation, remained for prolonged time periods. When glutamate was used to test excitability, 34% (16 of 47) of the enhancements lasted more than 5 min. When somatic stimuli were used 29% (15 of 52) lasted more than 5 min. With both measures some neurons still displayed enhanced responses more than 1 h after the treatment with ACh. 8. ACh appears to act as a permissive agent that allows modification of the effectiveness with which previously existing afferent inputs drive somatosensory cortical neurons. 9. This mechanism to alter neuronal responsiveness has many of the characteristics necessary to account for the reorganization observed in somatosensory cortex following alterations in its afferent drive and may be related to some forms of learning and memory.

scholarly journals Response Properties of Whisker-Related Neurons in Rat Second Somatosensory Cortex

2004 ◽  
Vol 92 (4) ◽  
pp. 2083-2092 ◽  
Author(s):  
Ernest E. Kwegyir-Afful ◽  
Asaf Keller
Keyword(s):  
Somatosensory Cortex ◽  
Receptive Fields ◽  
Stimulus Onset ◽  
Similar Response ◽  
Activity Levels ◽  
Response Latencies ◽  
Response Properties ◽  
Fast Spiking ◽  
Evoked Activity ◽  
Lemniscal System

In addition to a primary somatosensory cortex (SI), the cerebral cortex of all mammals contains a second somatosensory area (SII); however, the functions of SII are largely unknown. Our aim was to explore the functions of SII by comparing response properties of whisker-related neurons in this area with their counterparts in the SI. We obtained extracellular unit recordings from narcotized rats, in response to whisker deflections evoked by a piezoelectric device, and compared response properties of SI barrel (layer IV) neurons with those of SII (layers II to VI) neurons. Neurons in both cortical areas have similar response latencies and spontaneous activity levels. However, SI and SII neurons differ in several significant properties. The receptive fields of SII neurons are at least five times as large as those of barrel neurons, and they respond equally strongly to several principal whiskers. The response magnitude of SII neurons is significantly smaller than that of neurons in SI, and SII neurons are more selective for the angle of whisker deflection. Furthermore, whereas in SI fast-spiking (inhibitory) and regular-spiking (excitatory) units have different spontaneous and evoked activity levels and differ in their responses to stimulus onset and offset, SII neurons do not show significant differences in these properties. The response properties of SII neurons suggest that they are driven by thalamic inputs that are part of the paralemniscal system. Thus whisker-related inputs are processed in parallel by a lemniscal system involving SI and a paralemniscal system that processes complimentary aspects of somatosensation.

Plasticity of Primary Somatosensory Cortex Paralleling Sensorimotor Skill Recovery From Stroke in Adult Monkeys

1998 ◽  
Vol 79 (4) ◽  
pp. 2119-2148 ◽  
Author(s):  
Christian Xerri ◽  
Michael M. Merzenich ◽  
Bret E. Peterson ◽  
William Jenkins
Keyword(s):  
Somatosensory Cortex ◽  
Skill Acquisition ◽  
Cortical Area ◽  
Receptive Fields ◽  
Field Size ◽  
Primary Somatosensory Cortex ◽  
Small Object ◽  
Object Retrieval ◽  
Area 3A ◽  
Area 3B

Xerri, Christian, Michael M. Merzenich, Bret E. Peterson, and William Jenkins. Plasticity of primary somatosensory cortex paralleling sensorimotor skill recovery from stroke in adult monkeys. J. Neurophysiol. 79: 2119–2148, 1998. Adult owl and squirrel monkeys were trained to master a small-object retrieval sensorimotor skill. Behavioral observations along with positive changes in the cortical area 3b representations of specific skin surfaces implicated specific glabrous finger inputs as important contributors to skill acquisition. The area 3b zones over which behaviorally important surfaces were represented were destroyed by microlesions, which resulted in a degradation of movements that had been developed in the earlier skill acquisition. Monkeys were then retrained at the same behavioral task. They could initially perform it reasonably well using the stereotyped movements that they had learned in prelesion training, although they acted as if key finger surfaces were insensate. However, monkeys soon initiated alternative strategies for small object retrieval that resulted in a performance drop. Over several- to many-week-long period, monkeys again used the fingers for object retrieval that had been used successfully before the lesion, and reacquired the sensorimotor skill. Detailed maps of the representations of the hands in SI somatosensory cortical fields 3b, 3a, and 1 were derived after postlesion functional recovery. Control maps were derived in the same hemispheres before lesions, and in opposite hemispheres. Among other findings, these studies revealed the following 1) there was a postlesion reemergence of the representation of the fingertips engaged in the behavior in novel locations in area 3b in two of five monkeys and a less substantial change in the representation of the hand in the intact parts of area 3b in three of five monkeys. 2) There was a striking emergence of a new representation of the cutaneous fingertips in area 3a in four of five monkeys, predominantly within zones that had formerly been excited only by proprioceptive inputs. This new cutaneous fingertip representation disproportionately represented behaviorally crucial fingertips. 3) There was an approximately two times enlargement of the representation of the fingers recorded in cortical area 1 in postlesion monkeys. The specific finger surfaces employed in small-object retrieval were differentially enlarged in representation. 4) Multiple-digit receptive fields were recorded at a majority of emergent, cutaneous area 3a sites in all monkeys and at a substantial number of area 1 sites in three of five postlesion monkeys. Such fields were uncommon in area 1 in control maps. 5) Single receptive fields and the component fields of multiple-digit fields in postlesion representations were within normal receptive field size ranges. 6) No significant changes were recorded in the SI hand representations in the opposite (untrained, intact) control hemisphere. These findings are consistent with “substitution” and “vicariation” (adaptive plasticity) models of recovery from brain damage and stroke.

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.

scholarly journals Modular Processing in the Hand Representation of Primate Primary Somatosensory Cortex Coexists With Widespread Activation

2010 ◽  
Vol 104 (6) ◽  
pp. 3136-3145 ◽  
Author(s):  
Jamie L. Reed ◽  
Hui-Xin Qi ◽  
Pierre Pouget ◽  
Mark J. Burish ◽  
A. B. Bonds ◽  
...  
Keyword(s):  
Firing Rate ◽  
Somatosensory Cortex ◽  
Receptive Fields ◽  
Electrode Array ◽  
Electrode Site ◽  
Primary Somatosensory Cortex ◽  
Local Processing ◽  
Firing Rates ◽  
Area 3B ◽  
Activation Site

Neurons in the hand representation of primary somatosensory cortex (area 3b) are known to have discretely localized receptive fields; and these neurons form modules that can be visualized histologically as distinct digit and palm representations. Despite these indicators of the importance of local processing in area 3b, widespread interactions between stimuli presented to locations across the hand have been reported. We investigated the relationship of neuron firing rate with distance from the site of maximum activation in cortex by recording from a 100-electrode array with electrodes spaced 400 μm apart, implanted into the area 3b hand representation in anesthetized owl monkeys. For each stimulated location on the hand, the electrode site where neurons had the highest peak firing rate was defined as the peak activation site. The lesser firing rates of neurons at all other electrode sites in the grid were compared with the firing rates of neurons at the peak activation site. On average, peak firing rates of neurons decreased rapidly with distance away from the peak activation site. The effect of distance on the variance of firing rates was highly significant ( P < 0.0001). However, individual neurons retained high firing rates for distances over 3 mm. The clear decline in firing rate with distance from the most activated location indicates that local processing is emphasized in area 3b, while the distance of neurons with reduced but maintained firing rates ≤3–4 mm from the site of best activation demonstrated widespread activation in primary somatosensory cortex.

scholarly journals Somatosensory Cortex of Macaque Monkeys is Designed for Opposable Thumb

2020 ◽  
Author(s):  
Leslee Lazar ◽  
Prem Chand ◽  
Radhika Rajan ◽  
Hisham Mohammed ◽  
Neeraj Jain
Keyword(s):  
Somatosensory Cortex ◽  
Information Exchange ◽  
Tactile Stimulation ◽  
Precision Grip ◽  
Digital Information ◽  
Macaque Monkeys ◽  
Cortical Organization ◽  
Cortex Area ◽  
Cortical Inputs ◽  
Area 3B

AbstractThe evolution of opposable thumb has enabled fine grasping ability and precision grip, which led to the capacity for fine manipulation of objects and refined tool use. Since tactile inputs to an opposable thumb are often spatially and temporally out of synch with inputs from the fingers, we hypothesized that inputs from the opposable thumb would be processed in an independent module in the primary somatosensory cortex (area 3b). Here we show that in area 3b of macaque monkeys, most neurons in the thumb representation do not respond to tactile stimulation of other digits and receive few intrinsic cortical inputs from other digits. However, neurons in the representations of other digits respond to touch on any of the four digits and are significantly more interconnected in the cortex. The thumb inputs are thus processed in an independent module, whereas there is significantly more inter-digital information exchange between the other digits. This cortical organization reflects behavioral use of the hand with an opposable thumb.

Differential effects of the mode of touch, active and passive, on experience-driven plasticity in the S1 cutaneous digit representation of adult macaque monkeys

2020 ◽  
Vol 123 (3) ◽  
pp. 1072-1089
Author(s):  
Anita Cybulska-Klosowicz ◽  
François Tremblay ◽  
Wan Jiang ◽  
Stéphanie Bourgeon ◽  
El-Mehdi Meftah ◽  
...  
Keyword(s):  
Receptive Field ◽  
Somatosensory Cortex ◽  
Discrimination Task ◽  
Receptive Fields ◽  
Active Touch ◽  
Primary Somatosensory Cortex ◽  
Firing Rates ◽  
Passive Touch ◽  
Passive Exposure ◽  
Area 3B

This study compared the receptive field (RF) properties and firing rates of neurons in the cutaneous hand representation of primary somatosensory cortex (areas 3b, 1, and 2) of 9 awake, adult macaques that were intensively trained in a texture discrimination task using active touch (fingertips scanned over the surfaces using a single voluntary movement), passive touch (surfaces displaced under the immobile fingertips), or both active and passive touch. Two control monkeys received passive exposure to the same textures in the context of a visual discrimination task. Training and recording extended over 1–2 yr per animal. All neurons had a cutaneous receptive field (RF) that included the tips of the stimulated digits (D3 and/or D4). In area 3b, RFs were largest in monkeys trained with active touch, smallest in those trained with passive touch, and intermediate in those trained with both; i.e., the mode of touch differentially modified the cortical representation of the stimulated fingers. The same trends were seen in areas 1 and 2, but the changes were not significant, possibly because a second experience-driven influence was seen in areas 1 and 2, but not in area 3b: smaller RFs with passive exposure to irrelevant tactile inputs compared with recordings from one naive hemisphere. We suggest that added feedback during active touch and higher cortical firing rates were responsible for the larger RFs with behavioral training; this influence was tempered by periods of more restricted sensory feedback during passive touch training in the active + passive monkeys. NEW & NOTEWORTHY We studied experience-dependent sensory cortical plasticity in relation to tactile discrimination of texture using active and/or passive touch. We showed that neuronal receptive fields in primary somatosensory cortex, especially area 3b, are largest in monkeys trained with active touch, smallest in those trained with passive touch, and intermediate in those trained using both modes of touch. Prolonged, irrelevant tactile input had the opposite influence in areas 1 and 2, favoring smaller receptive fields.

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