Frequency discrimination training engaging a restricted skin surface results in an emergence of a cutaneous response zone in cortical area 3a

1992 ◽  
Vol 67 (5) ◽  
pp. 1057-1070 ◽  
Author(s):  
G. H. Recanzone ◽  
M. M. Merzenich ◽  
W. M. Jenkins
Keyword(s):  
Cortical Neurons ◽  
Cortical Area ◽  
Receptive Fields ◽  
Frequency Discrimination ◽  
Skin Surface ◽  
Opposite Hemisphere ◽  
Functional Roles ◽  
Area 3A ◽  
Cutaneous Response ◽  
Cortical Representations

1. The responses of cortical neurons evoked by cutaneous stimulation were investigated in the hand representation of cortical area 3a in adult owl monkeys that had been trained in a tactile frequency discrimination task. Cortical representations of the hands in these experimental hemispheres were compared with those representing the opposite, untrained hand, as well as with those representing a passively stimulated hand in a second class of control monkeys. 2. A large cutaneous representation of the hairy and glabrous skin surfaces of the hand emerged in area 3a in each trained hemisphere. 3. With the emergence of cutaneous responses recorded for neurons at many area 3a locations, the normally recorded deep receptor inputs were no longer evident at most of these locations. 4. There was a greater territory of representation of the small area of skin that was stimulated in the behavioral task in trained monkeys, when compared with the representations of corresponding skin sites in the opposite hemisphere of the same monkeys, or to the representations of equivalent skin sites stimulated in passively stimulated control monkeys. 5. There was great variability in the receptive-field properties of neurons responsive to cutaneous inputs among trained monkeys. In most recording sites within the representations of the behaviorally engaged hands, the cutaneous receptive fields were large, extending over a significant part of the glabrous or hairy surfaces of the hand. However, in one monkey, very small, topographically ordered cutaneous receptive fields were recorded over a wide zone of area 3a. 6. The physiologically defined borders between areas 3a and 3b were in register with the cytoarchitectonically defined borders between these two cortical areas in trained and in control monkeys. 7. This study demonstrates that there is a reorganization of the cutaneous and "deep" representation of hand in cortical area 3a, with the main change being an emergence of a large cutaneous representation and the parallel disappearance of a large part of the normal deep representation in this field. These changes are discussed in light of the possible functional roles of cortical area 3a.

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.

Physiological properties of neurons projecting from area 3a to area 4 gamma of feline cerebral cortex

1982 ◽  
Vol 48 (4) ◽  
pp. 1048-1057 ◽  
Author(s):  
H. Asanuma ◽  
R. S. Waters ◽  
H. Yumiya
Keyword(s):  
Cerebral Cortex ◽  
Motor Cortex ◽  
Cortical Neurons ◽  
Small Area ◽  
Receptive Fields ◽  
Projection Neurons ◽  
Intracortical Microstimulation ◽  
Projected Area ◽  
Physiological Properties ◽  
Area 3A

1. The corticocortical projection from area 3a to area 4 gamma was restudied using tranquilized cats. 2. Intracortical microstimulation (ICMS) of a given locus in area 3a produced effects on neurons in area 4 gamma that were located in a small area extending along the direction of the radial fibers constituting a columnar shape. 3. Cortical neurons in area 3a that projected to a particular neuron in area 4 gamma were located in a region that extended along the direction of the radial fibers and constituted a columnar shape. 4. Two-thirds of the projection neurons in area 3a had different receptive fields from those of neurons in the projected area in 4 gamma, thus suggesting that the 3a neurons are not simply transferring peripheral information to the 4 gamma neurons. 5. ICMS delivered to area 3a rarely excited 4 gamma neurons but rather facilitated their evoked discharges. 6. It is suggested that the activity of corticocortical projection from area 3a to 4 gamma can influence the activity of 4 gamma neurons only when combined with other inputs to the motor cortex.

Changes in the distributed temporal response properties of SI cortical neurons reflect improvements in performance on a temporally based tactile discrimination task

1992 ◽  
Vol 67 (5) ◽  
pp. 1071-1091 ◽  
Author(s):  
G. H. Recanzone ◽  
M. M. Merzenich ◽  
C. E. Schreiner
Keyword(s):  
Cortical Neurons ◽  
Cortical Area ◽  
Discrimination Task ◽  
Tactile Stimulus ◽  
Discrimination Performance ◽  
Frequency Discrimination ◽  
Temporal Response ◽  
Owl Monkeys ◽  
Control Skin ◽  
Area 3B

1. Temporal response characteristics of neurons were sampled in fine spatial grain throughout the hand representations in cortical areas 3a and 3b in adult owl monkeys. These monkeys had been trained to detect small differences in tactile stimulus frequencies in the range of 20-30 Hz. Stimuli were presented to an invariant, restricted spot on a single digit. 2. The absolute numbers of cortical locations and the cortical area over which neurons showed entrained frequency-following responses to behaviorally important stimuli were significantly greater when stimulation was applied to the trained skin, as compared with stimulation on an adjacent control digit, or at corresponding skin sites in passively stimulated control animals. 3. Representational maps defined with sinusoidal stimuli were not identical to maps defined with just-visible tapping stimuli. Receptive-field/frequency-following response site mismatches were recorded in every trained monkey. Mismatches were less frequently recorded in the representations of control skin surfaces. 4. At cortical locations with entrained responses, neither the absolute firing rates of neurons nor the degree of the entrainment of the response were correlated with behavioral discrimination performance. 5. All area 3b cortical locations with entrained responses evoked by stimulation at trained or untrained skin sites were combined to create population peristimulus time and cycle histograms. In all cases, stimulation of the trained skin resulted in 1) larger-amplitude responses, 2) peak responses earlier in the stimulus cycle, and 3) temporally sharper responses, than did stimulation applied to control skin sites. 6. The sharpening of the response of cortical area 3b neurons relative to the period of the stimulus could be accounted for by a large subpopulation of neurons that had highly coherent responses. 7. Analysis of cycle histograms for area 3b neuron responses revealed that the decreased variance in the representation of each stimulus cycle could account for behaviorally measured frequency discrimination performance. A strong correlation between these temporal response distributions and the discriminative performances for stimuli applied at all studied skin surfaces was even stronger (r = 0.98) if only the rising phases of cycle histogram were considered in the analysis. 8. The responses of neurons in area 3a could not account for measured differences in frequency discrimination performance. 9. These representational changes did not occur in monkeys that were stimulated on the same schedule but were performing an auditory discrimination task during skin stimulation. 10. It is concluded that by behaviorally training adult owl monkeys to discriminate the temporal features of a tactile stimulus, distributed spatial and temporal response properties of cortical neurons are altered.(ABSTRACT TRUNCATED AT 400 WORDS)

Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task

1992 ◽  
Vol 67 (5) ◽  
pp. 1031-1056 ◽  
Author(s):  
G. H. Recanzone ◽  
M. M. Merzenich ◽  
W. M. Jenkins ◽  
K. A. Grajski ◽  
H. R. Dinse
Keyword(s):  
Receptive Field ◽  
Cortical Neurons ◽  
Cortical Area ◽  
Receptive Fields ◽  
Field Size ◽  
Skin Site ◽  
Receptive Field Size ◽  
Topographic Complexity ◽  
Owl Monkeys ◽  
Area 3B

1. Adult owl monkeys were trained to detect differences in the frequency of a tactile flutter-vibration stimulus above a 20-Hz standard. All stimuli were delivered to a constant skin site restricted to a small part of a segment of one finger. The frequency-difference discrimination performance of all but one of these monkeys improved progressively with training. 2. The distributed responses of cortical neurons ("maps") of the hand surfaces were defined in detail in somatosensory cortical area 3b. Representations of trained hands were compared with those of the opposite, untrained hand, and to the area 3b representations of hands in a second set of monkeys that were stimulated tactually in the same manner while these monkeys were attending to auditory stimuli (passive stimulation controls). 3. The cortical representations of the trained hands were substantially more complex in topographic detail than the representations of unstimulated hands or of passively stimulated control hands. 4. In all well-trained monkeys the representations of the restricted skin location trained in the behavioral task were significantly (1.5 to greater than 3 times) greater in area than were the representations of equivalent skin locations on control digits. However, the overall extents of the representations of behaviorally stimulated fingers were not larger than those of control fingers in the same hemisphere, or in opposite hemisphere controls. 5. The receptive fields representing the trained skin were significantly larger than receptive fields representing control digits in all but one trained monkey. The largest receptive fields were centered in the zone of representation of the behaviorally engaged skin, but they were not limited to it. Large receptive fields were recorded in a 1- to 2-mm-wide zone in the area 3b maps of trained hands. 6. Receptive-field sizes were also statistically significantly larger on at least one adjacent, untrained digit when compared with the receptive fields recorded on the homologous digit of the opposite hand. 7. There was an increase in the percent overlaps of receptive fields in the cortical zone of representation of the trained skin. A significant number of receptive fields were centered on the behaviorally trained skin site. 8. The effects of increased topographic complexity, increased representation of the trained skin location, increased receptive-field size, and increased receptive-field overlap were not observed in the representations of the untrained hands in these same monkeys. Only modest increases in topographic complexity were recorded in the representations of passively stimulated hands, and no effects on receptive-field size or overlap were noted.(ABSTRACT TRUNCATED AT 400 WORDS)

Corticoreticular Pathways in the Cat. I. Projection Patterns and Collaterization

1998 ◽  
Vol 80 (1) ◽  
pp. 389-405 ◽  
Author(s):  
Bouchra Kably ◽  
Trevor Drew
Keyword(s):  
Receptive Field ◽  
Cortical Neurons ◽  
Cortical Area ◽  
Pyramidal Tract ◽  
Receptive Fields ◽  
Cortical Projection ◽  
Pericruciate Cortex ◽  
Conduction Velocities ◽  
Area 6 ◽  
The Face

Kably, Bouchra and Trevor Drew. Corticoreticular pathways in the cat. I. Projection patterns and collaterization. J. Neurophysiol. 80: 389–405, 1998. This paper summarizes and compares the projection patterns and the receptive fields of cortical neurons in areas 4 and 6 that project to the pontomedullary reticular formation (PMRF). A total of 326 neurons were recorded in area 4 and 129 in area 6 in four awake, unrestrained cats that were chronically implanted with arrays of electrodes in the PMRF and the pyramidal tract (PT). In area 4, 47% of the neurons projected to the caudal PT but not to the PMRF (PTNs); 19% were activated only from the PMRF [corticoreticular neurons (CRNs)], whereas 27% were activated from both the PT and the PMRF (PTN/CRNs). More PTN/CRNs conducted at velocities >20 m/s (82%) than did CRNs (23%). In area 6, only 19% of the neurons were identified as PTNs, 12% were PTN/CRNs and 31% were CRNs; a further 38% could not be activated from either structure. Collateral branches within the PMRF conducted at maximum velocities of 20 m/s (average = 6.5 m/s). No significant differences in the conduction velocities of the collateral branches were found either between fast and slow PTNs or between area 4 and area 6 neurons. A large proportion of neurons in area 4 (85/173, 49%) were activated by passive manipulation of the more distal, contralateral forelimb, with approximately equal numbers being classed as PTNs, PTN/CRNs and CRNs. Most neurons in area 6 for which a receptive field could be found were excited by lightly touching or tapping the face and neck; a receptive field could not be determined for 39% of the area 6 neurons compared with only 5% of those in area 4. Finally, there was evidence that neurons in quite widespread areas of the pericruciate cortex, including both areas 4 and 6 projected onto similar, restricted regions of the PMRF. The fact that the cortical projection from area 4 to the PMRF includes a high percentage of fast PTNs with a receptive field on the distal forelimb is consistent with the view that this projection may serve to integrate movement and the dynamic postural adjustments that accompany them. The fact that the cortical projection from area 6 to the PMRF is primarily from slow PTNs with receptive fields on the face, neck and back is consistent with a role for this cortical area in adjusting the general posture of the animal on which movements are superimposed.

scholarly journals Information diversity in individual auditory cortical neurons is associated with functionally distinct coordinated neuronal ensembles

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Jermyn Z. See ◽  
Natsumi Y. Homma ◽  
Craig A. Atencio ◽  
Vikaas S. Sohal ◽  
Christoph E. Schreiner
Keyword(s):  
Cortical Neurons ◽  
Single Neuron ◽  
Receptive Fields ◽  
Acoustic Feature ◽  
Neuronal Ensembles ◽  
Neuron Spike ◽  
Information Diversity ◽  
Feature Selectivity ◽  
Stimulus Features ◽  
Time Specific

AbstractNeuronal activity in auditory cortex is often highly synchronous between neighboring neurons. Such coordinated activity is thought to be crucial for information processing. We determined the functional properties of coordinated neuronal ensembles (cNEs) within primary auditory cortical (AI) columns relative to the contributing neurons. Nearly half of AI cNEs showed robust spectro-temporal receptive fields whereas the remaining cNEs showed little or no acoustic feature selectivity. cNEs can therefore capture either specific, time-locked information of spectro-temporal stimulus features or reflect stimulus-unspecific, less-time specific processing aspects. By contrast, we show that individual neurons can represent both of those aspects through membership in multiple cNEs with either high or absent feature selectivity. These associations produce functionally heterogeneous spikes identifiable by instantaneous association with different cNEs. This demonstrates that single neuron spike trains can sequentially convey multiple aspects that contribute to cortical processing, including stimulus-specific and unspecific information.

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.

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.

Responses of cortical neurons (areas 3a and 4) to ramp stretch of hindlimb muscles in the baboon

1976 ◽  
Vol 39 (3) ◽  
pp. 484-500 ◽  
Author(s):  
J. Hore ◽  
J. B. Preston ◽  
P. D. Cheney
Keyword(s):  
Cortical Neurons ◽  
Muscle Length ◽  
Muscle Afferents ◽  
Muscle Stretch ◽  
Hindlimb Muscles ◽  
Group I ◽  
Hindlimb Muscle ◽  
Area 3A ◽  
Group Ii Muscle Afferents ◽  
Group Ii

1. A study was made of the response of single cortical units in areas 3a and 4 to electrical stimulation of hindlimb muscle nerves and to ramp stretch of hindlimb muscles in baboons anesthetized with chloralose.2. Stimulation of hindlimb muscle nerves revealed a group I projection primarily to area 3a but with some input into adjacent area. 4. A major group II projection was found in area 4 adjacent to area 3a. A small number of area 3a neurons receive convergence from both group I and group II muscle afferents.3a. On the basis of their response pattern to ramp stretch, units were classified into one of six categories and their cytoarchitectonic location was determined. Units in area 3a had hynamic sensitivities equivalent to that of the primary spindle afferents. Although the discharge of some area 3a neurons also reflected differences in muscle length, most area 3a neurons had low position sensitivities. One unit type in area 3a did not respond to maintained muscle stretch and signaled only velocity of stretch.4. Units in area 4 had position sensitivities equivalent to that of primary and secondary spindle afferents. Although the discharge of some area 4 units reflected different velocities of muscle stretch, these units had dynamic sensitivities similar to those of secondary spindle afferents rather than those of primary afferents. One type of unit in area 4 had no dynamic component to muscle stretch and signaled only muscle length.5. The results demonstrate that there is a transfer of dynamic and position sensitivity from spindle afferents to cortical neurons. Furthermore, data processing has occurred because some units respond only to the steady-state length of muscle, while other units encode only the dynamic phase of stretch. This behavior is different from the responses to ramp stretch of either group I or group II muscle afferents in the baboon.6. The results demonstrate that single units in cerebral cortex can encode the information transmitted to the central nervous system by muscle spindle afferents. The purpose for which this information is used remains undetermined.

Sign in / Sign up

Export Citation Format

Share Document