Area 3b Hand Research Articles

Resting-State functional networks of different topographic representations in the somatosensory cortex of macaque monkeys and humans

Information processing in the brain is mediated through a complex functional network architecture whose comprising nodes integrate and segregate themselves on different timescales. To gain an understanding of the network function it is imperative to identify and understand the network structure with respect to the underlying anatomical connectivity and the topographic organization. Here we show that the previously described resting-state network for the somatosensory area 3b comprises of distinct networks that are characteristic for different topographic representations. Seed-based resting-state functional connectivity analysis in macaque monkeys and humans using BOLD-fMRI signals from the face, the hand and rest of the medial somatosensory representations of area 3b revealed different correlation patterns. Both monkeys and humans have many similarities in the connectivity networks, although the networks are more complex in humans with many more nodes. In both the species face area network has the highest ipsilateral and contralateral connectivity, which included areas 3b and 4, and ventral premotor area. The area 3b hand network included ipsilateral hand representation in area 4.The emergent functional network structures largely reflect the known anatomical connectivity. Our results show that different body part representations in area 3b have independent functional networks perhaps reflecting differences in the behavioral use of different body parts. The results also show that large cortical areas if considered together, do not give a complete and accurate picture of the network architecture.

Corticocuneate projections are altered after spinal cord dorsal column lesions in New World monkeys.

Recovery of responses to cutaneous stimuli in the area 3b hand cortex of monkeys after dorsal column lesions (DCLs) in the cervical spinal cord relies on neural rewiring in the cuneate nucleus (Cu) over time. To examine whether the corticocuneate projections are modified during recoveries after the DCL, we injected cholera toxin subunit B into the hand representation in Cu to label the cortical neurons after various recovery times, and related results to the recovery of neural responses in the affected area 3b hand cortex. In normal New World monkeys, labeled neurons were predominately distributed in the hand regions of contralateral areas 3b, 3a, 1 and 2, parietal ventral (PV), secondary somatosensory cortex (S2), and primary motor cortex (M1), with similar distributions in the ipsilateral cortex in significantly smaller numbers. In monkeys with short-term recoveries, the area 3b hand neurons were unresponsive or responded weakly to touch on the hand, while the cortical labeling pattern was largely unchanged. After longer recoveries, the area 3b hand neurons remained unresponsive, or responded to touch on the hand or somatotopically abnormal parts, depending on the lesion extent. The distributions of cortical labeled neurons were much more widespread than the normal pattern in both hemispheres, especially when lesions were incomplete. The proportion of labeled neurons in the contralateral area 3b hand cortex was not correlated with the functional reactivation in the area 3b hand cortex. Overall, our findings indicated that corticocuneate inputs increase during the functional recovery, but their functional role is uncertain.

Spatiotemporal trajectories of reactivation of somatosensory cortex by direct and secondary pathways after dorsal column lesions in squirrel monkeys

After lesions of the somatosensory dorsal column (DC) pathway, the cortical hand representation can become unresponsive to tactile stimuli, but considerable responsiveness returns over weeks of post-lesion recovery. The reactivation suggests that preserved subthreshold sensory inputs become potentiated and axon sprouting occurs over time to mediate recovery. Here, we studied the recovery process in 3 squirrel monkeys, using high-resolution cerebral blood volume-based functional magnetic resonance imaging (CBV-fMRI) mapping of contralateral somatosensory cortex responsiveness to stimulation of distal finger pads with low and high level electrocutaneous stimulation (ES) before and 2, 4, and 6weeks after a mid-cervical level contralateral DC lesion. Both low and high intensity ES of digits revealed the expected somatotopy of the area 3b hand representation in pre-lesion monkeys, while in areas 1 and 3a, high intensity stimulation was more effective in activating somatotopic patterns. Six weeks post-lesion, and irrespective of the severity of loss of direct DC inputs (98%, 79%, 40%), somatosensory cortical area 3b of all three animals showed near complete recovery in terms of somatotopy and responsiveness to low and high intensity ES. However there was significant variability in the patterns and amplitudes of reactivation of individual digit territories within and between animals, reflecting differences in the degree of permanent and/or transient silencing of primary DC and secondary inputs 2weeks post-lesion, and their spatio-temporal trajectories of recovery between 2 and 6weeks. Similar variations in the silencing and recovery of somatotopy and responsiveness to high intensity ES in areas 3a and 1 are consistent with individual differences in damage to and recovery of DC and spinocuneate pathways, and possibly the potentiation of spinothalamic pathways. Thus, cortical deactivation and subsequent reactivation depends not only on the degree of DC lesion, but also on the severity and duration of loss of secondary as well as primary inputs revealed by low and high intensity ES.

Intracortical connections are altered after long-standing deprivation of dorsal column inputs in the hand region of area 3b in squirrel monkeys.

A complete unilateral lesion of the dorsal column somatosensory pathway in the upper cervical spinal cord deactivates neurons in the hand region in contralateral somatosensory cortex (areas 3b and 1). Over weeks to months of recovery, parts of the hand region become reactivated by touch on the hand or face. To determine whether changes in cortical connections potentially contribute to this reactivation, we injected tracers into electrophysiologically identified locations in cortex of area 3b representing the reactivated hand and normally activated face in adult squirrel monkeys. Our results indicated that even when only partially reactivated, most of the expected connections of area 3b remained intact. These intact connections include the majority of intrinsic connections within area 3b; feedback connections from area 1, secondary somatosensory cortex (S2), parietal ventral area (PV), and other cortical areas; and thalamic inputs from the ventroposterior lateral nucleus (VPL). In addition, tracer injections in the reactivated hand region of area 3b labeled more neurons in the face and shoulder regions of area 3b than in normal monkeys, and injections in the face region of area 3b labeled more neurons in the hand region. Unexpectedly, the intrinsic connections within area 3b hand cortex were more widespread after incomplete dorsal column lesions (DCLs) than after a complete DCL. Although these additional connections were limited, these changes in connections may contribute to the reactivation process after injuries. J. Comp. Neurol. 524:1494-1526, 2016. © 2015 Wiley Periodicals, Inc.

Corticocortical projections to representations of the teeth, tongue, and face in somatosensory area 3b of macaques

We placed injections of anatomical tracers into representations of the tongue, teeth, and face in the primary somatosensory cortex (area 3b) of macaque monkeys. Our injections revealed strong projections to representations of the tongue and teeth from other parts of the oral cavity responsive region in 3b. The 3b face also provided input to the representations of the intraoral structures. The primary representation of the face showed a pattern of intrinsic connections similar to that of the mouth. The area 3b hand representation provided little to no input to either the mouth or the face representations. The mouth and face representations of area 3b received projections from the presumptive oral cavity and face regions of other somatosensory areas in the anterior parietal cortex and the lateral sulcus, including areas 3a, 1, 2, the second somatosensory area (S2), the parietal ventral area (PV), and cortex that may include the parietal rostral (PR) and ventral somatosensory (VS) areas. Additional inputs came from primary motor (M1) and ventral premotor (PMv) areas. This areal pattern of projections is similar to the well-studied pattern revealed by tracer injections in regions of 3b representing the hand. The tongue representation appeared to be unique in area 3b in that it also received inputs from areas in the anterior upper bank of the lateral sulcus and anterior insula that may include the primary gustatory area (area G) and other cortical taste-processing areas, as well as a region of lateral prefrontal cortex (LPFC) lining the principal sulcus.

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

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.

Thalamocortical connections of anterior and posterior parietal cortical areas in New World titi monkeys

We examined the thalamocortical connections of electrophysiologically identified locations in the hand and forelimb representations in areas 3b, 1, and 5 in the New World titi monkeys (Callicebus moloch), and of area 7b/AIP. Labeled cells and terminals in the thalamus resulting from the injections were related to architectonic boundaries. As in previous studies in primates, the hand representation of area 3b has dense, restricted projections predominantly from the lateral division of the ventral posterior nucleus (VPl). Projections to area 1 were highly convergent from several thalamic nuclei including the ventral lateral nucleus (VL), anterior pulvinar (PA), VPl, and the superior division of the ventral posterior nucleus (VPs). In cortex immediately caudal to area 1, what we term area 5, thalamocortical connections were also highly convergent and predominantly from nuclei of the thalamus associated with motor, visual, or somatic processing such as VL, the medial pulvinar (PM), and PA, respectively; with moderate projections from VP, central lateral nucleus (CL), lateral posterior nucleus (LP), and VPs. Finally, thalamocortical connections of area 7b/AIP were from a range of nuclei including PA, PM, LP/LD, VL, CL, PL, and CM. The current data support two conclusions drawn from previous studies in titi monkeys and other primates. First, cortex caudal to area 1 in New World monkeys is more like area 5 than area 2. Second, the presence of thalamic input to area 5 from both motor nuclei and somatosensory nuclei of the thalamus, suggests that area 5 could be considered a highly specialized sensorimotor area.

Hand/Face Border as a Limiting Boundary in the Body Representation in Monkey Somatosensory Cortex

Horizontal intracortical connections may form one substrate for representational plasticity in somatosensory cortex. Electrophysiological mapping demonstrated the finer details of the representations of the hand, lower jaw, neck, and face in area 3b of normal macaque monkeys. Injections of two fluorescent tracers then defined the extent to which horizontal connections crossed from the face into the hand representations and vice versa in area 3b. Connections are widely distributed within cortical representations of skin areas innervated by cervical nerves or by the trigeminal nerve but do not cross a border defined by the anterior limit of the representation of skin innervated by the second cervical nerve. This border separates the representation of the muzzle, innervated only by the mandibular nerve, and the representation of the lower jaw and neck region, innervated by the second and third cervical nerves but overlapped by the mandibular nerve. Thus, the muzzle representation lacks connections with the hand and with the lower jaw and neck representations, but the representations of the hand and of the lower jaw and neck are strongly interconnected. Overlap of the hand and of the lower jaw and neck representations and of their horizontal intracortical connections may form one basis for expansions of the lower jaw representation into that of the hand when peripheral input from the hand is lost. Lack of connections with the rest of the face representation may limit this spread.

Initial cortical reactions to injury of the median and radial nerves to the hands of adult primates.

The area 3b hand cortex of adult squirrel monkeys was mapped during the first minutes to hours after transecting the radial and median nerves to the hand. The objective was to evaluate initial cortical reactions to this injury and to determine whether patterns and extents of cortical change are similar in different individuals. There are 5 main findings. First, cortical aggregates related to ulnar nerve inputs from the hand rapidly expanded to occupy an additional 21% of the cortical hand map. Second, face and forearm inputs, which normally activate areas adjacent to hand cortex, rapidly expanded into areas of 4% and 1% of the hand cortex respectively. Third, cortical changes involved shifts in receptive field locations that were initiated within minutes after injury. Fourth, the spatial patterns and extents of cortical change were similar in different individuals. Finally, the pattern of cortical change produced after this injury differed from the pattern seen after injury of the median and ulnar nerves. These rapid expansions are a beginning point from which further changes must progress; however, in contrast to changes accompanying chronic hand injuries, these initial cortical reactions do not appear dictated by use of uninjured inputs.

Sensory afferent projections and area 3b somatotopy following median nerve cut and repair in macaque monkeys.

The fidelity of median nerve regeneration and the consequent effects of regeneration errors on cortical organization were determined in combined anatomical and electrophysiological studies. In three adult macaque monkeys, the median nerve was cut, sutured, and allowed to regenerate for 7-13 months. After regeneration, distributions of afferents to the dorsal horn of the spinal cord and the cuneate nucleus of the brainstem were determined by making injections of horseradish peroxidase conjugates into the distal phalanges of digit 1 or 2. While label from a single digit on the normal hand was confined to the appropriate locations in the median nerve territories of the dorsal horn and cuneate nucleus, label from the reinnervated digits spread out to cover most of the median nerve territories in those structures. These results are consistent with the interpretation that some proportion of primary sensory fibers normally innervating other digits and pads of median nerve skin erroneously reinnervated the skin of the injected digits. In the same monkeys, microelectrodes were used to record from an array of closely spaced sites across the representation of the hand in area 3b of somatosensory cortex. The reactivation pattern was abnormal, with neurons at many recording sites having more than one receptive field, larger than normal receptive fields, or receptive fields at abnormal skin locations. Thus, there is somatotopic disorder both in the regenerated median nerve and in reactivated cortex, indicating that primary somatosensory cortex does not reorganize to compensate fully for peripheral reinnervation errors in these adult primates. Nevertheless, the organization of receptive fields in area 3b suggests the existence of some central selection of synapses.

The consistency, extent, and locations of early-onset changes in cortical nerve dominance aggregates following injury of nerves to primate hands

The somatosensory cortex of primates contains patch- and bandlike aggregates of neurons that are dominantly activated by cutaneous inputs from the radial, median, and ulnar nerves to the hand. In the present study, the area 3b hand cortex of adult monkeys was mapped immediately before and after combined median and ulnar nerve transection to evaluate the consistency, extent, and location of early post-injury alterations in the deprived median and ulnar nerve cortical bands. Several alterations were observed acutely after injury. (1) The patchlike cortical aggregates of intact radial nerve inputs from the hand underwent a two- to three-fold expansion. This expansion was not related to peripheral changes in the radial nerve skin territory, but was due to rapid central decompression of radial nerve dominance patches. (2) The largest changes involved patches in lateral to central locations of the hand map. (3) The expanded patches occupied cortical zones that were activated by inputs from the digits, palm, and posterior hand prior to injury. These receptive field shifts were initiated within minutes after injury. (4) Receptive fields of neurons within expanded radial nerve patches were normal in size. (5) Besides changes involving radial nerve inputs from the hand, there was a small expansion of forelimb inputs into the preinjury hand cortex; however, the representation of face inputs did not expand into this cortex. (6) Finally, neurons across 50-69% of the hand cortex were unresponsive to tactile stimuli acutely after this injury. These findings indicate that the distribution patterns of nerve dominance aggregates in adult primates begin changing within minutes after nerve injury. Cortical changes involving specific inputs occupy similar extents and locations of cortex, and are arranged in highly consistent patterns, in different individuals. It is suggested that this consistency reflects specific patterns of central sensitization or disinhibition that are triggered by the injury.

Changes in the cortical map of the hand following postnatal ulnar and radial nerve injury in monkeys: organization and modification of nerve dominance aggregates

The ulnar and radial nerves to the hands of 12-31-d-old marmoset monkeys were transected and ligated, and the monkeys were subsequently reared for periods of 1.4-1.6 years with only median nerve innervation to the hand. Features of organization in the cortical area 3b hand map were then assessed with neurophysiological mapping procedures, and compared to features in monkeys that had undergone either a normal postnatal development with three intact hand nerves, or an abnormal development with two intact nerves due to postnatal injury of the median nerve. A systematic comparison of cortical organization in these monkeys led to three main findings. First, some features of organization show little or no change when monkeys are reared with one, two, or three hand nerves. These features include receptive field size and the overall size of the hand map. Second, other features are, in contrast, clearly altered in an injury-dependent manner. These features include cortical neuronal thresholds to light tactile stimuli, and the spatial location, size, shape, continuity, and somatotopic interfacing of representations of the parts of the hand. Finally, estimates of the peripheral innervation territories of the hand nerves, and of the corresponding distributions of cortical neurons activated by inputs from these territories, indicate that the normal hand map contains bandlike aggregates of neurons that are dominantly activated by inputs from each nerve. Postnatal nerve injuries alter the size of these nerve dominance aggregates.

Changes in the cortical map of the hand following postnatal median nerve injury in monkeys: modification of somatotopic aggregates

Median nerves to the hands of 8-15-d-old marmoset monkeys were transected and precluded from regeneration by ligation. Following periods of 0.4-1.5 years, features of organization in the cortical area 3b hand map were assessed neurophysiologically, and compared to features in normally reared monkeys. Cortical features in monkeys with both histories were similar in certain respects. (1) Receptive field organization was similar in terms of tactile thresholds and receptive field size, continuity, and glabrous-hairy specificity. (2) Somatotopic organization was similar in terms of the continuity of the glabrous representation, and progressions of receptive field shifts across some parts of the hand map. (3) Finally, the overall size of the hand map did not change. In contrast, other cortical features clearly differed following these developmental histories. (1) Neurons at virtually all recording sites in normal hand maps responded to light mechanical stimulation, whereas, following injury, neurons at about 8% of the recording sites responded only to high-intensity stimuli. (2) Somatotopic organization differed in terms of the presence or absence of the representation of skin autonomously innervated by the median nerve, the number and continuity of representations of hairy skin, and the spatial interfacing of representations. (3) Finally, there were differences in the areas and widths of representations of parts of the hand. The overall impression is that there is a correspondence between the cortical features that changed most after injury, and the features that varied most in individual normal monkeys: in both circumstances the most variable features involved properties of spatial patterning across large aggregates of neurons as reflected by the size, shape, continuity, and interfacing of representations. A hypothesis is proposed that suggests that the cortical hand map normally consists of a number of representations that are capable of developing and surviving somewhat autonomously of each other. The features of spatial patterning in the mosaiclike map of these representations are influenced by postnatal availability of inputs from intact hand nerves.

Ablations of Areas 3b (SI Proper) and 3a of Somatosensory Cortex in Marmosets Deactivate the Second and Parietal Ventral Somatosensory Areas

Partial ablations of specific parts of cortical areas 3b (SI proper) and 3a in marmosets were found to render somatotopically equivalent parts of two other cortical somatosensory fields, the second somatosensory area (SII) and the parietal ventral area (PV), unresponsive to peripheral stimulation. Microelectrode recordings in anesthetized marmosets first established the responsiveness and locations of the representations of body parts, including the hand in areas 3a and 3b, SII, and in some cases PV. The hand representations in areas 3a and 3b were then removed by aspiration. Immediately afterwards, additional recordings established that regions of SII and PV that formerly represented the hand were no longer responsive to cutaneous stimulation of the hand (or any other skin surface). Other parts of these fields, representing parts of the body other than the hand, remained responsive to stimulation of the previously effective receptive fields. We conclude that SII and PV depend on inputs (either direct or indirect) from areas 3a and 3b for their activation.

The arbors of axons terminating in middle cortical layers of somatosensory area 3b in owl monkeys.

The arbors of single axons terminating predominantly in layer IV of the representation of the hand in area 3b of owl monkeys were reconstructed from serial brain sections after axons beneath the cortex were severed and horseradish peroxidase was injected into the white matter. In addition to dense terminations in layer IV, these labeled axons generally had branches extending into deeper layer III, and a few had very sparse terminations in layer VI. Terminal arbors ranged from 100 to 900 microns in diameter, and fine branches with synaptic boutons were unevenly distributed, typically grouped in a large central cluster and one or more smaller side clusters. The results are consistent with three broad conclusions: (1) Since the arbors are large relative to the details of the somatotopic map in area 3b, all regions within a single arbor may not be equally effective in activating cortical cells. (2) Spatially separate branches of single axons may relate to spatially separate modules of neurons of the same class in a manner that allows them to receive the same inputs. (3) Many of the somatotopic changes that have been reported in the hand representation as a result of nerve manipulations in adults could result from alterations in synaptic effectiveness within the arbors of single axons.

Consistent features of the representation of the hand in area 3b of macaque monkeys.

Multiunit microelectrode recordings were used to explore the responsiveness and somatotopic organization of the representation of the hand in area 3b of anesthetized macaque monkeys. Major findings were as follows: Recording sites throughout the hand representation were activated by low-threshold cutaneous stimulation. Simple, punctate mechanical stimuli were highly effective in activating neurons. Neurons had small, restricted receptive fields. Representations of nearly all skin surfaces of the hand were demonstrated in individual monkeys. The basic topographic pattern found in all monkeys included the following: a large sequential representation of the glabrous digits from thumb to little finger from lateral to medial in cortex, and from proximal to distal hand parts in cortex extending down the caudal bank of the central sulcus; moderately large representations of radial and ulnar pads of the palm in respective lateral and medial cortical locations in the hand representation; and a relatively small, fragmented representation of the dorsal hand and dorsal digits, with the fragments interspersed within the representation of the glabrous hand. The proportions of the proximal, middle, and distal glabrous digits varied, so that the representation of the distal phalanx sometimes approached the dorsal border of area 3b with area 1. A comparison of the present findings with previous results from macaque monkeys indicates that the above-described features have been revealed under a variety of recording and anesthetic conditions. Consistencies in previous and present results strongly support the conclusions that the hand representation in area 3b of macaque monkeys is activated by cutaneous receptors throughout; is composed of neurons with relatively simple, small, cutaneous receptive fields; includes all skin surfaces of the hand; and is somatotopic for the glabrous skin with small, discontinuous, intercalated representations of fragments of the dorsal skin.

Functional reorganization in somatosensory cortical areas 3b and 1 of adult monkeys after median nerve repair: possible relationships to sensory recovery in humans

Previous studies have shown that the primary somatosensory cortex of adult mammals undergoes somatotopic reorganization in response to peripheral nerve transection. The present study assesses how cortical organization is affected when a transected nerve subsequently regenerates. The median nerve to one hand of adult owl monkeys was transected and repaired. Following nerve regeneration, the representations of the hand in cortical areas 3b and 1 were studied with neurophysiological mapping methods. The major results were as follows: Peripherally, median nerve transection, repair, and regeneration resulted in reinnervation of the median nerve skin territory. Centrally, both the initial loss and subsequent regeneration of median nerve inputs caused reorganizational changes in cortex. Reorganizational changes were specifically restricted to regions of the hand cortex where inputs from the median nerve were normally represented. The functional features of cortical regions that recovered tactile responsiveness from reinnervated skin regions were abnormal in several respects. Most notably, these regions contained recording sites with abnormally located or multiple cutaneous receptive fields, and contained major topographical changes, such as reestablishment of palmar pad or digit representations in small, discontinuous patches of cortex. Normal organizational features were reestablished to a more limited extent. These features included recovery of delimited, discrete receptive fields and reestablishment of topographic representations for localized skin areas. Different transformations in topographical organization were seen in areas 3b and 1 of the same monkey. These results suggest that nerve regeneration reestablishes the cortical capacity to process tactile information from reinnervated skin via a prolonged reorganizational process that appears dependent on peripheral and central factors. Cortical recovery mechanisms clearly appear to have limitations, since preinjury patterns of cortical organization are not widely recovered even almost 1 year after repair. We suggest possible relationships between cortical reorganizational changes in these primates, and postrepair sensory changes in humans.

Somatosensory cortical map changes following digit amputation in adult monkeys.

The cortical representations of the hand in area 3b in adult owl monkeys were defined with use of microelectrode mapping techniques 2-8 months after surgical amputation of digit 3, or of both digits 2 and 3. Digital nerves were tied to prevent their regeneration within the amputation stump. Successive maps were derived in several monkeys to determine the nature of changes in map organization in the same individuals over time. In all monkeys studied, the representations of adjacent digits and palmar surfaces expanded topographically to occupy most or all of the cortical territories formerly representing the amputated digit(s). With the expansion of the representations of these surrounding skin surfaces (1) there were severalfold increases in their magnification and (2) roughly corresponding decreases in receptive field areas. Thus, with increases in magnification, surrounding skin surfaces were represented in correspondingly finer grain, implying that the rule relating receptive field overlap to separation in distance across the cortex (see Sur et al., '80) was dynamically maintained as receptive fields progressively decreased in size. These studies also revealed that: the discontinuities between the representations of the digits underwent significant translocations (usually by hundreds of microns) after amputation, and sharp new discontinuous boundaries formed where usually separated, expanded digital representations (e.g., of digits 1 and 4) approached each other in the reorganizing map, implying that these map discontinuities are normally dynamically maintained. Changes in receptive field sizes with expansion of representations of surrounding skin surfaces into the deprived cortical zone had a spatial distribution and time course similar to changes in sensory acuity on the stumps of human amputees. This suggests that experience-dependent map changes result in changes in sensory capabilities. The major topographic changes were limited to a cortical zone 500-700 micron on either side of the initial boundaries of the representation of the amputated digits. More distant regions did not appear to reorganize (i.e., were not occupied by inputs from surrounding skin surfaces) even many months after amputation. The representations of some skin surfaces moved in entirety to locations within the former territories of representation of amputated digits in every monkey studied. In man, no mislocation errors or perceptual distortions result from stimulation of surfaces surrounding a digital amputation.(ABSTRACT TRUNCATED AT 400 WORDS)

Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys

In an earlier study ( Neuroscience 8, 33–55, 1983), we found that the cortex representing the skin of the median nerve within parietal somatosensory fields 3b and 1 was completely occupied by ‘new’ inputs from the ulnar and radial nerves, 2–9 months after the median nerve was cut and tied in adult squirrel and owl monkeys. In this report, we describe the results of studies directed toward determining the time course and likely mechanisms underlying this remarkable plasticity. Highly detailed maps of the hand surface representation were derived in monkeys before, immediately after, and at subsequent short and intermediate time stages after median nerve section. In one monkey, maps were derived before nerve section, immediately after nerve section, and 11, 22 and 144 days later. Thus, direct comparisons in cortical map structure could be made over time in this individual monkey. In other experiments, single maps were derived at given post-section intervals. These studies revealed that: (1) large cortical sectors were ‘silenced’ by median nerve transection. (2) Significant inputs restricted to the dorsum of the radial hand and the dorsum of digits 1, 2 and 3 were immediately ‘unmasked’ by median nerve transection. (3) These immediately ‘unmasked’ regions were topographically crude, and represented only fragments of this dorsal skin. They were transformed, over time, into very large, highly topographic and complete representations of dorsal skin surfaces. (4) Representations of bordering glabrous skin surfaces progressively expanded to occupy larger and larger portions of the former median nerve cortical representational zone. (5) These ‘expanded’ representations of ulnar nerve-innervated skin surfaces sometimes moved, in entirety, into the former median nerve representational zone. (6) Almost all of the former median nerve zone was driven by new inputs in a map derived 22 days after nerve section. At shorter times (3, 6 and 11 days), ‘reoccupation’ was still incomplete. (7) Very significant changes in map dimensions within and outside of the former median skin cortical field were seen after the ‘reoccupation’ of the deprived cortex by ‘new’ inputs was initially completed. (8) Progressive changes were recorded within the original ulnar and radial nerve cortical representational zones, as skin surfaces originally overtly represented wholly within these regions expanded into the former median nerve zone. (9) Throughout the studied period, the cortical representational loci of many skin sites appeared to change continually and often markedly. (10) The locations of map discontinuities also shifted significantly over time. (11) Concommitant with changes in representational magnification over time, inverse changes in receptive field sizes were recorded. (12) Immediately ‘unmasked’ inputs had greater than normal receptive field overlap as a function of distance across the cortical surface. The normal ‘hypercolumn’ rule 67 was progressively re-established. (13) The topographical progression of reorganization and ultimate reorganizational patterns differed greatly in Areas 3b and 1. The evident capacity for change in and around the deprived cortical zone of: (a) cortical map dimensions; (b) cortical sites of representation of different skin surfaces (obversely, the skin surfaces represented at given cortical sites over time) (c) receptive field sizes and overlaps (d) of the locations of map discontinuities clearly demonstrates that details of cortical map structure in Areas 3b and 1 are dynamically maintained. The present studies indicate that nerve transection results in both immediate and progressively developing changes in the cortical maps of this skin surface. While some portions of the deprived cortex were not cutaneously responsive immediately after transection, other parts of this cortex were immediately activated by ‘new’ cutaneous inputs. The reoccupation of the deprived cortex gradually increased, and dramatic changes in somatotopic organization occurred even after initial complete reactivation. Changes in receptive field sizes were seen concurrent with changes in somatotopic organization. These results have important implications for consideration of the nature of reorganization processes. They provide further, strong evidence that the detailed structure of the manifest somatotopic cortical organization is dynamically maintained. They bear implications for consideration of the significance and of the nature of physiologically recorded topographic representations of sensory epithelia in normal monkeys.

Dose- and time-dependent effects of ketamine on SI neurons with cutaneous receptive fields.

Dose- and time-dependent effects of ketamine on SI neurons with cutaneous receptive fields.G H Duncan, D A Dreyer, T M McKenna, and B L WhitselG H Duncan, D A Dreyer, T M McKenna, and B L WhitselPublished Online:01 Apr 1982https://doi.org/10.1152/jn.1982.47.4.677MoreSectionsPDF (4 MB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformation Cited ByDifferential effects of the mode of touch, active and passive, on experience-driven plasticity in the S1 cutaneous digit representation of adult macaque monkeysAnita Cybulska-Klosowicz, François Tremblay, Wan Jiang,† Stéphanie Bourgeon, El-Mehdi Meftah, and C. Elaine Chapman23 March 2020 | Journal of Neurophysiology, Vol. 123, No. 3Isoflurane and ketamine differentially influence spontaneous and evoked laminar electrophysiology in mouse V1Nicholas J. Michelson and Takashi D. Y. Kozai24 October 2018 | Journal of Neurophysiology, Vol. 120, No. 5Functional neuroimaging studies of human somatosensory cortexBehavioural Brain Research, Vol. 135, No. 1-2Optical imaging of intrinsic signals in somatosensory cortexBehavioural Brain Research, Vol. 135, No. 1-2Fine-Scale Organization of SI (Area 3b) in the Squirrel Monkey Revealed With Intrinsic Optical ImagingLi Min Chen, Robert M. Friedman, Benjamin M. Ramsden, Robert H. LaMotte, and Anna Wang Roe1 December 2001 | Journal of Neurophysiology, Vol. 86, No. 6Response Properties and Organization of Nociceptive Neurons in Area 1 of Monkey Primary Somatosensory CortexDan R. Kenshalo, Koichi Iwata, Maurice Sholas, and David A. Thomas1 August 2000 | Journal of Neurophysiology, Vol. 84, No. 2Surround Suppression in the Responses of Primate SA1 and RA Mechanoreceptive Afferents Mapped with a Probe ArrayF. Vega-Bermudez, and K. O. Johnson1 June 1999 | Journal of Neurophysiology, Vol. 81, No. 6SI Neuron Response Variability Is Stimulus Tuned and NMDA Receptor DependentB. L. Whitsel, O. Favorov, K. A. Delemos, C.-J. Lee, M. Tommerdahl, G. K. Essick, and B. Nakhle1 June 1999 | Journal of Neurophysiology, Vol. 81, No. 6Multisensory Integration in the Superior Colliculus of the Alert CatMark T. Wallace, M. Alex Meredith, and Barry E. Stein1 August 1998 | Journal of Neurophysiology, Vol. 80, No. 2Correlation of Effects of General Anesthetics on Somatosensory Neurons in the Primate Thalamus and Cortical EEG PowerP. M. Dougherty, Y. J. Li, F. A. Lenz, L. Rowland, and S. Mittman1 March 1997 | Journal of Neurophysiology, Vol. 77, No. 3Set related and premovement related activity of primate primary somatosensory cortical neurons depends upon stimulus modality and subsequent movementBrain Research Bulletin, Vol. 21, No. 3Neurons without demonstrable receptive fields outnumber neurons having receptive fields in samples from the somatosensory cortex of anesthetized or paralyzed cats and ratsBrain Research, Vol. 440, No. 1Influence of anesthesia on spontaneous activity and receptive field size of single units in rat Sm1 neocortexExperimental Neurology, Vol. 99, No. 2Spatial organization of the peripheral input to area 1 cell columns. I. the detection of ‘segregates’Brain Research Reviews, Vol. 13, No. 1Spatial organization of the peripheral input to area 1 cell columns. II. The forelimb representation achieved by a mosaic of segregatesBrain Research Reviews, Vol. 13, No. 1Intrinsic neocortical organization: Some comparative aspectsNeuroscience, Vol. 18, No. 1Metabolic labeling associated with index finger stimulation in monkey SI: Between animal variabilityBrain Research, Vol. 342, No. 2Somatosensory cortex in macaque monkeys: laminar differences in receptive field size in areas 3b and 1Brain Research, Vol. 342, No. 2Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeysNeuroscience, Vol. 10, No. 3Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentationNeuroscience, Vol. 8, No. 1 More from this issue > Volume 47Issue 4April 1982Pages 677-99 https://doi.org/10.1152/jn.1982.47.4.677PubMed7069461History Published online 1 April 1982 Published in print 1 April 1982 Metrics