scholarly journals Reorganization of Higher-Order Somatosensory Cortex After Sensory Loss from Hand in Squirrel Monkeys

2018 ◽  
Vol 29 (10) ◽  
pp. 4347-4365 ◽  
Author(s):  
Hui-Xin Qi ◽  
Chia-Chi Liao ◽  
Jamie L Reed ◽  
Jon H Kaas

Abstract Unilateral dorsal column lesions (DCL) at the cervical spinal cord deprive the hand regions of somatosensory cortex of tactile activation. However, considerable cortical reactivation occurs over weeks to months of recovery. While most studies focused on the reactivation of primary somatosensory area 3b, here, for the first time, we address how the higher-order somatosensory cortex reactivates in the same monkeys after DCL that vary across cases in completeness, post-lesion recovery times, and types of treatments. We recorded neural responses to tactile stimulation in areas 3a, 3b, 1, secondary somatosensory cortex (S2), parietal ventral (PV), and occasionally areas 2/5. Our analysis emphasized comparisons of the responsiveness, somatotopy, and receptive field size between areas 3b, 1, and S2/PV across DCL conditions and recovery times. The results indicate that the extents of the reactivation in higher-order somatosensory areas 1 and S2/PV closely reflect the reactivation in primary somatosensory cortex. Responses in higher-order areas S2 and PV can be stronger than those in area 3b, thus suggesting converging or alternative sources of inputs. The results also provide evidence that both primary and higher-order fields are effectively activated after long recovery times as well as after behavioral and electrocutaneous stimulation interventions.

2018 ◽  
Vol 115 (16) ◽  
pp. 4258-4263 ◽  
Author(s):  
Chia-Chi Liao ◽  
Jamie L. Reed ◽  
Hui-Xin Qi ◽  
Eva K. Sawyer ◽  
Jon H. Kaas

Months after the occurrence of spinal cord dorsal column lesions (DCLs) at the cervical level, neural responses in the hand representation of somatosensory area 3b hand cortex recover, along with hand use. To examine whether the second-order spinal cord pathway contributes to this functional recovery, we injected cholera toxin subunit B (CTB) into the hand representation in the cuneate nucleus (Cu) to label the spinal cord neurons, and related results to cortical reactivation in four squirrel monkeys (Saimiri boliviensis) at least 7 months after DCL. In two monkeys with complete DCLs, few CTB-labeled neurons were present below the lesion, and few neurons in the affected hand region in area 3b responded to touch on the hand. In two other cases with large but incomplete DCLs, CTB-labeled neurons were abundant below the lesion, and the area 3b hand cortex responded well to tactile stimulation in a roughly somatotopic organization. The proportions of labeled neurons in the spinal cord hand region reflected the extent of cortical reactivation to the hand. Comparing monkeys with short and long recovery times suggests that the numbers of labeled neurons below the lesion increase with time following incomplete DCLs (<95%) but decrease with time after nearly complete DCLs (≥95%). Taken together, these results suggest that the second-order spinal cord pathway facilitates cortical reactivation, likely through the potentiation of persisting tactile inputs from the hand to the Cu over months of postlesion recovery.


1998 ◽  
Vol 79 (4) ◽  
pp. 2119-2148 ◽  
Author(s):  
Christian Xerri ◽  
Michael M. Merzenich ◽  
Bret E. Peterson ◽  
William Jenkins

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.


1989 ◽  
Vol 62 (3) ◽  
pp. 711-722 ◽  
Author(s):  
T. Allison ◽  
G. McCarthy ◽  
C. C. Wood ◽  
P. D. Williamson ◽  
D. D. Spencer

1. The anatomic generators of human median nerve somatosensory evoked potentials (SEPs) in the 40 to 250-ms latency range were investigated in 54 patients by means of cortical-surface and transcortical recordings obtained during neurosurgery. 2. Contralateral stimulation evoked three groups of SEPs recorded from the hand representation area of sensorimotor cortex: P45-N80-P180, recorded anterior to the central sulcus (CS) and maximal on the precentral gyrus; N45-P80-N180, recorded posterior to the CS and maximal on the postcentral gyrus; and P50-N90-P190, recorded near and on either side of the CS. 3. P45-N80-P180 inverted in polarity to N45-P80-N180 across the CS but was similar in polarity from the cortical surface and white matter in transcortical recordings. These spatial distributions were similar to those of the short-latency P20-N30 and N20-P30 potentials described in the preceding paper, suggesting that these long-latency potentials are generated in area 3b of somatosensory cortex. 4. P50-N90-P190 was largest over the anterior one-half of somatosensory cortex and did not show polarity inversion across the CS. This spatial distribution was similar to that of the short-latency P25-N35 potentials described in the preceding paper and, together with our and Goldring et al. 1970; Stohr and Goldring 1969 transcortical recordings, suggest that these long-latency potentials are generated in area 1 of somatosensory cortex. 5. SEPs of apparently local origin were recorded from several regions of sensorimotor cortex to stimulation of the ipsilateral median nerve. Surface and transcortical recordings suggest that the ipsilateral potentials are generated not in area 3b, but rather in other regions of sensorimotor cortex perhaps including areas 4, 1, 2, and 7. This spatial distribution suggests that the ipsilateral potentials are generated by transcallosal input from the contralateral hemisphere. 6. Recordings from the periSylvian region were characterized by P100 and N100, recorded above and below the Sylvian sulcus (SS) respectively. This distribution suggests a tangential generator located in the upper wall of the SS in the second somatosensory area (SII). In addition, N125 and P200, recorded near and on either side of the SS, suggest a radial generator in a portion of SII located in surface cortex above the SS. 7. In comparison with the short-latency SEPs described in the preceding paper, the long-latency potentials were more variable and were more affected by intraoperative conditions.


1986 ◽  
Vol 56 (6) ◽  
pp. 1475-1497 ◽  
Author(s):  
P. Herron ◽  
R. Dykes

The ventroposterior region of the thalamus of mongrel cats was searched to locate zones activated by somatic stimuli. By using stimuli that selectively excited Pacinian corpuscles, areas activated by this class of afferent fibers were differentiated from regions activated by other classes of cutaneous mechanoreceptors. The results showed that Pacinian inputs excite neurons in the ventroposterior inferior nucleus (VPI) of the thalamus, whereas other more dorsal zones within the ventroposterior thalamus receive inputs from other mechanoreceptor classes. This definition of the VPI tended to be larger and to extend further lateral than some published descriptions. Horseradish peroxidase (HRP) was injected into ventroposterior zones shown by electrophysiological recordings to receive inputs from Pacinian afferents. Subsequently, labeled cell bodies were observed in the caudal poles of the dorsal column nuclei, a region previously shown to be activated by Pacinian afferents. Very few labeled cells were found in the central region of these nuclei, a region previously shown to be activated by other classes of cutaneous mechanoreceptors. Electrophysiological recordings were used to locate a small portion of the second somatosensory cortex driven by Pacinian stimuli. When HRP was injected into this region cell bodies in the VPI and the lateral part of the posterior group were labeled, but few or no labeled cells were found in ventroposterior lateral nucleus. We hypothesize that the VPI receives Pacinian information from a cytoarchitecturally distinct region in the caudal poles of the dorsal column nuclei. Further, we suggest that a major cortical target for the VPI is a subdivision of the second somatosensory cortex. These studies do not exclude the possibility that Pacinian inputs have other thalamic and cortical targets.


2019 ◽  
Author(s):  
Robert G. Law ◽  
Sarah Pugliese ◽  
Hyeyoung Shin ◽  
Danielle Sliva ◽  
Shane Lee ◽  
...  

AbstractTransient neocortical events with high spectral power in the 15–29Hz beta band are among the most reliable predictors of sensory perception: High prestimulus beta event rates in primary somatosensory lead to sensory suppression, most effective at 100–300ms prestimulus latency. However, the synaptic and neuronal mechanisms inducing beta’s perceptual effects have not been completely localized. We combined human MEG with neural modeling designed to account for these macroscale signals to interpret the cellular and circuit mechanisms that underlie the influence of beta on tactile detection. Extending prior studies, we modeled the hypothesis that higher-order thalamic bursts, sufficient for beta event generation in cortex, recruit supragranular GABAB inhibition acting on a 300ms time scale to suppress sensory information. Consistency between model and MEG data supported this hypothesis and led to a further prediction, validated in our data, that stimuli are perceived when beta events occur simultaneously with tactile stimulation. The post-event suppressive mechanism explains an array of studies that associate beta with decreased processing, while the during-event mechanism may demand a reinterpretation of the role of beta events in the context of coincident timing.Significance statementSomatosensory beta events – transient 15-29Hz oscillations in electromagnetic recordings – are thought to be generated when “top-down” bursts of spikes presumably originating in higher-order thalamus arrive in upper layers of somatosensory cortex. Physiological evidence had shown that the immediate action of these top-down projections should be excitatory; however, after a beta event, sensory perception is noticeably inhibited for approximately 300ms. The source of this post-event sensory suppression, in particular, had been unresolved. Using a detailed computational model of somatosensory cortex, we find evidence for the hypothesis that these bursts couple indirectly to GABAB inhibition in upper layers of cortex, and that beta events first briefly disinhibit sensory relay before a longer period of inhibition.


Sign in / Sign up

Export Citation Format

Share Document