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.

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.

Spatio-Temporal Subthreshold Receptive Fields in the Vibrissa Representation of Rat Primary Somatosensory Cortex

1998 ◽  
Vol 80 (6) ◽  
pp. 2882-2892 ◽  
Author(s):  
Christopher I. Moore ◽  
Sacha B. Nelson
Keyword(s):  
Receptive Field ◽  
Somatosensory Cortex ◽  
Rise Time ◽  
Cortical Plasticity ◽  
Temporal Dynamics ◽  
Receptive Fields ◽  
Excitatory Input ◽  
Primary Somatosensory Cortex ◽  
Spatio Temporal ◽  
Sensory Evoked

Moore, Christopher I. and Sacha B. Nelson. Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J. Neurophysiol. 80: 2882–2892, 1998. Whole cell recordings of synaptic responses evoked by deflection of individual vibrissa were obtained from neurons within adult rat primary somatosensory cortex. To define the spatial and temporal properties of subthreshold receptive fields, the spread, amplitude, latency to onset, rise time to half peak amplitude, and the balance of excitation and inhibition of subthreshold input were quantified. The convergence of information onto single neurons was found to be extensive: inputs were consistently evoked by vibrissa one- and two-away from the vibrissa that evoked the largest response (the “primary vibrissa”). Latency to onset, rise time, and the incidence and strength of inhibitory postsynaptic potentials (IPSPs) varied as a function of position within the receptive field and the strength of evoked excitatory input. Nonprimary vibrissae evoked smaller amplitude subthreshold responses [primary vibrissa, 9.1 ± 0.84 (SE) mV, n = 14; 1-away, 5.1 ± 0.5 mV, n = 38; 2-away, 3.7 ± 0.59 mV, n = 22; 3-away, 1.3 ± 0.70 mV, n = 8] with longer latencies (primary vibrissa, 10.8 ± 0.80 ms; 1-away, 15.0 ± 1.2 ms; 2-away, 15.7 ± 2.0 ms). Rise times were significantly faster for inputs that could evoke action potential responses (suprathreshold, 4.1 ± 1.3 ms, n = 8; subthreshold, 12.4 ± 1.5 ms, n = 61). In a subset of cells, sensory evoked IPSPs were examined by deflecting vibrissa during injection of hyperpolarizing and depolarizing current. The strongest IPSPs were evoked by the primary vibrissa ( n = 5/5), but smaller IPSPs also were evoked by nonprimary vibrissae ( n = 8/13). Inhibition peaked by 10–20 ms after the onset of the fastest excitatory input to the cortex. This pattern of inhibitory activity led to a functional reversal of the center of the receptive field and to suppression of later-arriving and slower-rising nonprimary inputs. Together, these data demonstrate that subthreshold receptive fields are on average large, and the spatio-temporal dynamics of these receptive fields vary as a function of position within the receptive field and strength of excitatory input. These findings constrain models of suprathreshold receptive field generation, multivibrissa interactions, and cortical plasticity.

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.

Acute changes in cutaneous receptive fields in primary somatosensory cortex after digit denervation in adult flying fox

1991 ◽  
Vol 65 (2) ◽  
pp. 178-187 ◽  
Author(s):  
M. B. Calford ◽  
R. Tweedale
Keyword(s):  
Receptive Field ◽  
Somatosensory Cortex ◽  
Receptive Fields ◽  
Acute Effect ◽  
Primary Somatosensory Cortex ◽  
Inhibitory Influence ◽  
Large Area ◽  
Acute Changes ◽  
Short Time ◽  
Flying Fox

1. Acute effects of permanent and temporary denervation of the flying fox thumb were examined to test the hypothesis that a large area of skin around the cutaneous receptive field of multiunits (MRF) at a locus in primary somatosensory cortex (SI) supplies viable inputs which can be rapidly unmasked by interruption of the dominant input from the area of the MRF. 2. The immediate effect of amputation of the thumb at loci where the original receptive field was entirely removed was to produce large MRFs on adjacent body areas (wrist, forearm, prowing, and finger membranes). Greatly expanded MRFs were also produced when amputation removed only part of the original MRF at a cortical locus. 3. The probable source of input to account for the new receptive fields is the extensive arborization of ascending projections within the somatosensory pathway, which supply a cortical locus with a potential input from a far larger area than is represented in its normal receptive field. The rapidity with which new or expanded fields are seen following denervation indicates that the normally unexpressed inputs around a receptive field are not only potential inputs but are inherently viable. Hence the most likely explanation for the results of this study is that the effect of the denervation is to disrupt an inhibitory influence that normally has the role of shaping the receptive field. 4. Temporary anesthesia of all or part of a MRF produced similar initial effects to amputation. When responsiveness returned to the locally anesthetized area (after 10-30 min), an expanded MRF persisted for a short time after which the boundaries of the MRF shrank. This rapid reversal suggests that a mechanistic rather than a plastic change is the basis for the acute effect of a small denervation on SI.

scholarly journals A touch of hierarchy: population receptive fields reveal fingertip integration in Brodmann areas in human primary somatosensory cortex

2021 ◽  
Author(s):  
W. Schellekens ◽  
M. Thio ◽  
S. Badde ◽  
J. Winawer ◽  
N. Ramsey ◽  
...  
Keyword(s):  
Receptive Field ◽  
Somatosensory Cortex ◽  
Receptive Fields ◽  
Body Part ◽  
Field Size ◽  
Primary Somatosensory Cortex ◽  
Vibrotactile Stimulation ◽  
Brodmann Areas ◽  
Functional Hierarchy ◽  
Stimulation Of

AbstractSeveral neuroimaging studies have shown the somatotopy of body part representations in primary somatosensory cortex (S1), but the functional hierarchy of distinct subregions in human S1 has not been adequately addressed. The current study investigates the functional hierarchy of cyto-architectonically distinct regions, Brodmann areas BA3, BA1, and BA2, in human S1. During functional MRI experiments, we presented participants with vibrotactile stimulation of the fingertips at three different vibration frequencies. Using population Receptive Field (pRF) modeling of the fMRI BOLD activity, we identified the hand region in S1 and the somatotopy of the fingertips. For each voxel, the pRF center indicates the finger that most effectively drives the BOLD signal, and the pRF size measures the spatial somatic pooling of fingertips. We find a systematic relationship of pRF sizes from lower-order areas to higher-order areas. Specifically, we found that pRF sizes are smallest in BA3, increase slightly towards BA1, and are largest in BA2, paralleling the increase in visual receptive field size as one ascends the visual hierarchy. Additionally, we find that the time-to-peak of the hemodynamic response in BA3 is roughly 0.5 s earlier compared to BA1 and BA2, further supporting the notion of a functional hierarchy of subregions in S1. These results were obtained during stimulation of different mechanoreceptors, suggesting that different afferent fibers leading up to S1 feed into the same cortical hierarchy.

Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons

1984 ◽  
Vol 52 (6) ◽  
pp. 1066-1093 ◽  
Author(s):  
R. W. Dykes ◽  
P. Landry ◽  
R. Metherate ◽  
T. P. Hicks
Keyword(s):  
Receptive Field ◽  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Receptive Fields ◽  
Field Size ◽  
Primary Somatosensory Cortex ◽  
Gamma Aminobutyric Acid ◽  
Receptive Field Size ◽  
Thalamic Stimulation ◽  
Somatosensory Neurons

Extracellular recordings of 209 neurons were obtained with carbon fiber-containing multibarrel micropipettes. The cells were isolated in the primary somatosensory cortex of cats anesthetized with barbiturate and classified according to the nature of their response to natural stimuli, the nature of the surrounding multiunit responses to the same stimuli, the response to thalamic stimulation, and their depth in the cortex. To study factors controlling the excitability of somatosensory neurons, their receptive fields were examined in the presence of iontophoretically administered gamma-aminobutyric acid (GABA), glutamate, and bicuculline methiodide (BMI). Even when the neurons were depolarized to perithreshold levels with glutamate, or when local inhibitory influences mediated by GABA were antagonized by BMI, the apparent specificity for one class of afferent input was maintained. Neurons responding to stimulation of either cutaneous or deep receptors maintained their modality specificity, and neurons in cutaneous rapidly adapting regions never took on slowly adapting properties. When ejected at currents that did not elicit action potentials, glutamate lowered the threshold for activation by cutaneous stimuli but did not enlarge the receptive field. With larger ejecting currents, the neurons developed an on-going discharge, but even at these higher doses, glutamate did not produce an increase in the receptive-field size. Some neurons in regions of cortex exhibiting slowly adapting multiunit responses were relatively insensitive to glutamate. These cells required four to five times more glutamate to evoke discharges than did most neurons. Other cells, previously unresponsive to somatic stimuli, could be shown to possess distinct cutaneous receptive fields when either glutamate or BMI was ejected in their vicinity. Iontophoretically administered BMI altered the firing pattern of somatosensory neurons, causing them to discharge in bursts of 3-15 impulses. BMI enlarged the receptive-field size of neurons in regions displaying rapidly adapting multiunit background discharges but not in those regions with slowly adapting multiunit discharges. This differential effect of BMI, suggesting that GABA controls receptive-field size in rapidly adapting regions, also indicates that neurons in rapidly adapting regions differ pharmacologically from those in other submodality regions. In all cortical regions, BMI blocked the poststimulus inhibitory period that normally followed thalamic stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)

Tactile activity in primate primary somatosensory cortex during active arm movements: cytoarchitectonic distribution

1994 ◽  
Vol 71 (1) ◽  
pp. 173-181 ◽  
Author(s):  
M. J. Prud'homme ◽  
D. A. Cohen ◽  
J. F. Kalaska
Keyword(s):  
Somatosensory Cortex ◽  
Receptive Fields ◽  
Arm Movements ◽  
Primary Somatosensory Cortex ◽  
Tactile Stimuli ◽  
Low Threshold ◽  
Deep Activity ◽  
Area 3B

1. Cells were recorded in areas 3b and 1 of the primary somatosensory cortex (SI) of three monkeys during active arm movements. Successful reconstructions were made of 46 microelectrode penetrations, and 298 cells with tactile receptive fields (RFs) were located as to cytoarchitectonic area, lamina, or both. 2. Area 3b contained a greater proportion of cells with slowly adapting responses to tactile stimuli and fewer cells with deep modality inputs than did area 1. Area 3b also showed a greater level of movement-related modulation in tactile activity than area 1. Other cell properties were equally distributed in the two areas. 3. The distribution of cells with low-threshold tactile RFs that also responded to lateral stretch of the skin or to passive arm movements was skewed toward deeper laminae than for tactile cells that did not respond to those manipulations. 4. The variation of activity of tactile neurons during arm movements in different directions was weaker in the superficial laminae than in deeper cortical laminae. 5. Cells with only increases in activity during arm movements were preferentially but not exclusively located in middle and superficial layers. Cells with reciprocal responses were found mainly in laminae III and V, whereas cells with only decreases in activity were concentrated in lamina V. 6. Overall, active arm movements evoke directionally tuned tactile and “deep” activity in areas 3b and 1, in particular in the deeper cortical laminae that are the source of the descending output pathways from SI.

scholarly journals A touch of hierarchy. Population Receptive Fields reveal fingertip integration in Brodmann areas in human primary somatosensory cortex

2021 ◽  
Author(s):  
W. Schellekens ◽  
M. Thio ◽  
S. Badde ◽  
J. Winawer ◽  
N. Ramsey ◽  
...  
Keyword(s):  
Receptive Field ◽  
Somatosensory Cortex ◽  
Receptive Fields ◽  
Body Part ◽  
Field Size ◽  
Primary Somatosensory Cortex ◽  
Vibrotactile Stimulation ◽  
Brodmann Areas ◽  
Functional Hierarchy ◽  
Stimulation Of

AbstractSeveral neuroimaging studies have shown the somatotopy of body part representations in primary somatosensory cortex (S1), but the functional hierarchy of distinct subregions in human S1 has not been adequately addressed. The current study investigates the functional hierarchy of cyto-architectonically distinct regions, Brodmann areas BA3, BA1, and BA2, in human S1. During functional MRI experiments, we presented participants with vibrotactile stimulation of the fingertips at 3 different vibration frequencies. Using population Receptive Field (pRF) modeling of the fMRI BOLD activity, we identified the hand region in S1 and the somatotopy of the fingertips. For each voxel, the pRF center indicates the finger that most effectively drives the BOLD signal, and the pRF size measures the spatial somatic pooling of fingertips. We find a systematic relationship of pRF sizes from lower-order areas to higher-order areas. Specifically, we found that pRF sizes are smallest in BA3, increase slightly towards BA1, and are largest in BA2, paralleling the increase in visual receptive field size as one ascends the visual hierarchy. Additionally, we find that the time-to-peak of the hemodynamic response in BA3 is roughly 0.5s earlier compared to BA1 and BA2, further supporting the notion of a functional hierarchy of subregions in S1. These results were obtained during stimulation of different mechanoreceptors, suggesting that different afferent fibers leading up to S1 feed into the same cortical hierarchy.

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