Structure of Receptive Fields in Area 3b of Primary Somatosensory Cortex in the Alert Monkey

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.

Download Full-text

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

Journal of Neurophysiology ◽

10.1152/jn.00566.2010 ◽

2010 ◽

Vol 104 (6) ◽

pp. 3136-3145 ◽

Cited By ~ 12

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.

Download Full-text

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

Journal of Neurophysiology ◽

10.1152/jn.00014.2019 ◽

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.

Download Full-text

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

Journal of Neurophysiology ◽

10.1152/jn.1994.71.1.173 ◽

1994 ◽

Vol 71 (1) ◽

pp. 173-181 ◽

Cited By ~ 20

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.

Download Full-text

Faculty Opinions recommendation of Optical imaging of a tactile illusion in area 3b of the primary somatosensory cortex.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1016771.211559 ◽

2004 ◽

Author(s):

Corinna Darian-Smith

Keyword(s):

Optical Imaging ◽

Somatosensory Cortex ◽

Primary Somatosensory Cortex ◽

Tactile Illusion ◽

Area 3B

Download Full-text

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

Journal of Neurophysiology ◽

10.1152/jn.1998.80.6.2882 ◽

1998 ◽

Vol 80 (6) ◽

pp. 2882-2892 ◽

Cited By ~ 214

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.

Download Full-text

Structure of the Excitatory Receptive Fields of Infragranular Forelimb Neurons in the Rat Primary Somatosensory Cortex Responding To Touch

Cerebral Cortex ◽

10.1093/cercor/bhj023 ◽

2005 ◽

Vol 16 (6) ◽

pp. 791-810 ◽

Cited By ~ 28

Author(s):

Banu Tutunculer ◽

Guglielmo Foffani ◽

B. Timothy Himes ◽

Karen A. Moxon

Keyword(s):

Somatosensory Cortex ◽

Receptive Fields ◽

Primary Somatosensory Cortex

Download Full-text

Nonoverlapping Thalamocortical Connections to Normal and Deprived Primary Somatosensory Cortex for Similar Forelimb Receptive Fields in Chronic Spinal Cats

Somatosensory Research ◽

10.3109/07367228809144633 ◽

1988 ◽

Vol 5 (4) ◽

pp. 311-323 ◽

Cited By ~ 14

Author(s):

Patricia A. McKinley ◽

Lawrence Kruger

Keyword(s):

Somatosensory Cortex ◽

Receptive Fields ◽

Primary Somatosensory Cortex ◽

Thalamocortical Connections

Download Full-text

Computational Role of Large Receptive Fields in the Primary Somatosensory Cortex

Journal of Neurophysiology ◽

10.1152/jn.01015.2007 ◽

2008 ◽

Vol 100 (1) ◽

pp. 268-280 ◽

Cited By ~ 29

Author(s):

Guglielmo Foffani ◽

John K. Chapin ◽

Karen A. Moxon

Keyword(s):

Somatosensory Cortex ◽

Receptive Fields ◽

Spike Timing ◽

Spike Count ◽

Primary Somatosensory Cortex ◽

Single Neurons ◽

Tuning Curves ◽

Tactile Stimuli ◽

Somatosensory Information

Computational studies are challenging the intuitive view that neurons with broad tuning curves are necessarily less discriminative than neurons with sharp tuning curves. In the context of somatosensory processing, broad tuning curves are equivalent to large receptive fields. To clarify the computational role of large receptive fields for cortical processing of somatosensory information, we recorded ensembles of single neurons from the infragranular forelimb/forepaw region of the rat primary somatosensory cortex while tactile stimuli were separately delivered to different locations on the forelimbs/forepaws under light anesthesia. We specifically adopted the perspective of individual columns/segregates receiving inputs from multiple body location. Using single-trial analyses of many single-neuron responses, we obtained two main results. 1) The responses of even small populations of neurons recorded from within the same estimated column/segregate can be used to discriminate between stimuli delivered to different surround locations in the excitatory receptive fields. 2) The temporal precision of surround responses is sufficiently high for spike timing to add information over spike count in the discrimination between surround locations. This surround spike-timing code (i) is particularly informative when spike count is ambiguous, e.g., in the discrimination between close locations or when receptive fields are large, (ii) becomes progressively more informative as the number of neurons increases, (iii) is a first-spike code, and (iv) is not limited by the assumption that the time of stimulus onset is known. These results suggest that even though large receptive fields result in a loss of spatial selectivity of single neurons, they can provide as a counterpart a sophisticated temporal code based on latency differences in large populations of neurons without necessarily sacrificing basic information about stimulus location.

Download Full-text