Large-Scale Reorganization in the Somatosensory Cortex and Thalamus after Sensory Loss in Macaque Monkeys
TL;DR: A comparison of the extents of deafferentation across the monkeys shows that even if the dorsal column lesion is partial, preserving most of the hand representation, it is sufficient to induce an expansion of the face representation.
Abstract: Adult brains undergo large-scale plastic changes after peripheral and central injuries. Although it has been shown that both the cortical and thalamic representations can reorganize, uncertainties exist regarding the extent, nature, and time course of changes at each level. We have determined how cortical representations in the somatosensory area 3b and the ventroposterior (VP) nucleus of thalamus are affected by long standing unilateral dorsal column lesions at cervical levels in macaque monkeys. In monkeys with recovery periods of 22-23 months, the intact face inputs expanded into the deafferented hand region of area 3b after complete or partial lesions of the dorsal columns. The expansion of the face region could extend all the way medially into the leg and foot representations. In the same monkeys, similar expansions of the face representation take place in the VP nucleus of the thalamus, indicating that both these processing levels undergo similar reorganizations. The receptive fields of the expanded representations were similar in somatosensory cortex and thalamus. In two monkeys, we determined the extent of the brain reorganization immediately after dorsal column lesions. In these monkeys, the deafferented regions of area 3b and the VP nucleus became unresponsive to the peripheral touch immediately after the lesion. No reorganization was seen in the cortex or the VP nucleus. A comparison of the extents of deafferentation across the monkeys shows that even if the dorsal column lesion is partial, preserving most of the hand representation, it is sufficient to induce an expansion of the face representation.
Citations
More filters
TL;DR: It is proposed that the traditional concept of the body schema should be divided into three components: primary somatosensory representations, which are representations of the skin surface that are typically somatotopically organized, and have been shown to change dynamically due to peripheral or central modifications.
185 citations
01 Jan 2012
TL;DR: The unique anatomy of the pathway for facial sensations, involving the trigeminal ganglion and its associated nuclei within the brainstem, and the opportunities that this offers for training and rehabilitation are addressed.
Abstract: This chapter addresses the unique anatomy of the pathway for facial sensations, involving the trigeminal ganglion and its associated nuclei within the brainstem. The innervation of specialized cranial structures such as the teeth, tongue, oral and nasal mucosa, cornea, meninges, and conjunctiva are considered. This chapter will also address trigeminal mechanisms in clinically relevant conditions such as toothache, headache and trigeminal neuralgia including using advances in imaging techniques and resolution. Thus it is now possible to obtain functional MR images (fMRI) of the trigeminal pathway from ganglion to cortex. Magnetoencephalography (MEG) and fMRI techniques have provided more details on cortical organization in facial regions of both S1 and S2, while diffusion tensor imaging has been useful for visualizing trigeminothalamic pathways. Plasticity of the system after injury, its association with pain conditions, and the opportunities that this offers for training and rehabilitation, are further areas of current research that are discussed.
179 citations
TL;DR: The brain’s ability to reorganise itself is key to the authors' recovery from injuries, but the subsequent mismatch between old and new organisation may lead to pain, so a ‘maladaptive plasticity’ theory is argued against by showing that phantom pain in upper limb amputees is independent of cortical remapping.
Abstract: The role of cortical activity in generating and abolishing chronic pain is increasingly emphasized in the clinical community. Perhaps the most striking example of this is the maladaptive plasticity theory, according to which phantom pain arises from remapping of cortically neighbouring representations (lower face) into the territory of the missing hand following amputation. This theory has been extended to a wide range of chronic pain conditions, such as complex regional pain syndrome. Yet, despite its growing popularity, the evidence to support the maladaptive plasticity theory is largely based on correlations between pain ratings and oftentimes crude measurements of cortical reorganization, with little consideration of potential contributions of other clinical factors, such as adaptive behaviour, in driving the identified brain plasticity. Here, we used a physiologically meaningful measurement of cortical reorganization to reassess its relationship to phantom pain in upper limb amputees. We identified small yet consistent shifts in lip representation contralateral to the missing hand towards, but not invading, the hand area. However, we were unable to identify any statistical relationship between cortical reorganization and phantom sensations or pain either with this measurement or with the traditional Euclidian distance measurement. Instead, we demonstrate that other factors may contribute to the observed remapping. Further research that reassesses more broadly the relationship between cortical reorganization and chronic pain is warranted.
148 citations
Cites background from "Large-Scale Reorganization in the S..."
...…in the primary somatosensory cortex (SI), where the lower face representation takes over the cortical territory of the missing hand (Pons et al., 1991; Jain et al., 2008) (see Devor and Wall, 1978; Florence and Kaas, 1995; Kambi et al., 2014 for reorganization in subcortical structures)....
[...]
TL;DR: It is suggested that acute stroke activates unique pathways that can rapidly redistribute function within the spared cortical hemisphere within 30–50 min of stroke onset, and not merely loss of activity.
Abstract: Most processing of sensation involves the cortical hemisphere opposite (contralateral) to the stimulated limb. Stroke patients can exhibit changes in the interhemispheric balance of sensory signal processing. It is unclear whether these changes are the result of poststroke rewiring and experience, or whether they could result from the immediate effect of circuit loss. We evaluated the effect of mini-strokes over short timescales (<2 h) where cortical rewiring is unlikely by monitoring sensory-evoked activity throughout much of both cortical hemispheres using voltage-sensitive dye imaging. Blockade of a single pial arteriole within the C57BL6J mouse forelimb somatosensory cortex reduced the response evoked by stimulation of the limb contralateral to the stroke. However, after stroke, the ipsilateral (uncrossed) forelimb response within the unaffected hemisphere was spared and became independent of the contralateral forelimb cortex. Within the unaffected hemisphere, mini-strokes in the opposite hemisphere significantly enhanced sensory responses produced by stimulation of either contralateral or ipsilateral pathways within 30-50 min of stroke onset. Stroke-induced enhancement of responses within the spared hemisphere was not reproduced by inhibition of either cortex or thalamus using pharmacological agents in nonischemic animals. I/LnJ acallosal mice showed similar rapid interhemispheric redistribution of sensory processing after stroke, suggesting that subcortical connections and not transcallosal projections were mediating the novel activation patterns. Thalamic inactivation before stroke prevented the bilateral rearrangement of sensory responses. These findings suggest that acute stroke, and not merely loss of activity, activates unique pathways that can rapidly redistribute function within the spared cortical hemisphere.
135 citations
TL;DR: It is shown that a complete thoracic transection of the spinal cord produces immediate functional reorganization in the primary somatosensory cortex of anesthetized rats, and that this state change plays a critical role in the early cortical reorganization after spinal cord injury.
Abstract: Spinal cord injury can produce extensive long-term reorganization of the cerebral cortex. Little is known, however, about the sequence of cortical events starting immediately after the lesion. Here we show that a complete thoracic transection of the spinal cord produces immediate functional reorganization in the primary somatosensory cortex of anesthetized rats. Besides the obvious loss of cortical responses to hindpaw stimuli (below the level of the lesion), cortical responses evoked by forepaw stimuli (above the level of the lesion) markedly increase. Importantly, these increased responses correlate with a slower and overall more silent cortical spontaneous activity, representing a switch to a network state of slow-wave activity similar to that observed during slow-wave sleep. The same immediate cortical changes are observed after reversible pharmacological block of spinal cord conduction, but not after sham. We conclude that the deafferentation due to spinal cord injury can immediately (within minutes) change the state of large cortical networks, and that this state change plays a critical role in the early cortical reorganization after spinal cord injury.
132 citations
Cites background from "Large-Scale Reorganization in the S..."
...…can lead to major long-term reorganization of cortical topographic maps, reflecting remarkable plasticity in the adult brain (Wall and Egger, 1971; Jain et al., 1997, 2008; Bruehlmeier et al., 1998; Green et al., 1998; Curt et al., 2002; Endo et al., 2007; Ghosh et al., 2009, 2010; Tandon et al.,…...
[...]
References
More filters
TL;DR: Reorganization of brainstem and thalamic nuclei associated with slow transneuronal atrophy is likely to be a progressive process and when coupled with divergence of ascending connections, it islikely to make a substantial contribution to representational changes in cortex.
Abstract: After long-term denervation of an upper limb in macaque monkeys, the representation of the face in somatosensory cortex expands over many millimeters into the silenced representation of the hand. Various brainstem and cortical mechanisms have been proposed to explain this phenomenon. Reorganization in the thalamus has been largely ignored. In monkeys with deafferented upper limbs for 12 to 20 years, it was found that the brainstem cuneate and the thalamic ventral posterior nuclei had undergone severe transneuronal atrophy, and physiological mapping in the thalamus revealed that the face and trunk representations were adjoined while the normally small representation of the lower face had expanded comparable to the expansion in cortex. Reorganization of brainstem and thalamic nuclei associated with slow transneuronal atrophy is likely to be a progressive process. When coupled with divergence of ascending connections, it is likely to make a substantial contribution to representational changes in cortex.
246 citations
"Large-Scale Reorganization in the S..." refers background or result in this paper
...…previous reports from monkeys suggest mostly similar reorganizations in the VP nucleus and area 3b (Jones, 1983, 2000; Garraghty and Kaas, 1991a; Jones and Pons, 1998) differences have been reported (Florence et al., 2001), which could be because of shaping of the receptive fields at each level…...
[...]
...Similar changes also took place in the VP nucleus, although they were accompanied by gross morphological changes, attributed to transneuronal degenerations (Jones and Pons, 1998)....
[...]
...Although previous reports from monkeys suggest mostly similar reorganizations in the VP nucleus and area 3b (Jones, 1983, 2000; Garraghty and Kaas, 1991a; Jones and Pons, 1998) differences have been reported (Florence et al....
[...]
TL;DR: Analysis of first- and higher-order properties of spontaneous neuronal activity revealed that spike trains could be classified into two groups with distinct patterns of activity.
Abstract: 1. We explored the region of the principal sensory nucleus of thalamus (Vc) during stereotactic surgical procedures for treatment of patients with pain after spinal cord transection (n = 23). Recep...
246 citations
"Large-Scale Reorganization in the S..." refers background in this paper
...In patients with spinal cord injuries at thoracic levels there was an expansion of the body region just proximal to the deafferented part (Lenz et al., 1994)....
[...]
TL;DR: The 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.
Abstract: 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.
243 citations
"Large-Scale Reorganization in the S..." refers background in this paper
...Following partial loss of hand inputs because of nerve cut or digit amputations there is “filling in” by the remaining hand inputs (Merzenich et al., 1983b, 1984; Wall et al., 1986; Garraghty et al., 1994); and after upper or lower limb amputations, representation of the skin of the limb proximal to the amputation expands (Lenz et al....
[...]
TL;DR: The result suggests that the thalamic plasticity that is seen immediately after a peripheral deafferentation is dependent upon both descending corticofugal projections and ascending trigeminothalamic projections.
Abstract: Multiple neuron ensemble recordings were obtained simultaneously from both the primary somatosensory (SI) cortex and the ventroposterior medial thalamus (VPM) before and during the combined administration of reversible inactivation of the SI cortex and a reversible subcutaneous block of peripheral trigeminal nerve fibers. This procedure was performed to quantify the contribution of descending corticofugal projections on (i) the normal organization of thalamic somatosensory receptive fields and (ii) the thalamic somatosensory plastic reorganization that immediately follows a peripheral deafferentation. Reversible inactivation of SI cortex resulted in immediate changes in receptive field properties throughout the VPM. Cortical inactivation also significantly reduced but did not completely eliminate the occurrence of VPM receptive field reorganization resulting from the reversible peripheral deafferentation. This result suggests that the thalamic plasticity that is seen immediately after a peripheral deafferentation is dependent upon both descending corticofugal projections and ascending trigeminothalamic projections.
218 citations
"Large-Scale Reorganization in the S..." refers background in this paper
..., 2001), which could be because of shaping of the receptive fields at each level by complex interactions of the divergent feedforward and feedback connections (Ergenzinger et al., 1998; Krupa et al., 1999)....
[...]
...…and Kaas, 1991a; Jones and Pons, 1998) differences have been reported (Florence et al., 2001), which could be because of shaping of the receptive fields at each level by complex interactions of the divergent feedforward and feedback connections (Ergenzinger et al., 1998; Krupa et al., 1999)....
[...]
TL;DR: The findings suggest that cortical representations of deafferented skin can become activated by substitute cutaneous inputs, and suggests these changes are due to functional modifications in normally existing connections.
Abstract: The hindpaw of the rat is normally innervated by the sciatic and saphenous nerves. In the present studies, the hindpaws of adult rats were partially deafferented by transection of the sciatic nerve for variable periods of time. The organization of the hindpaw representation in primary somatosensory (S-I) cortex was then studied with neurophysiological mapping techniques and compared to the organization seen in normal rats. The objective was to determine whether cutaneous responsiveness was recovered in the cortical area which lost normal cutaneous inputs from the sciatic nerve, and, if recovery occurred, to characterize the time course and spatial extent of this recovery. Normal rats were found to have a topographically organized representation of the hindpaw in S-I cortex. As determined by nerve recording and cortical mapping, approximately 85% of this representation is responsive to cutaneous inputs from the sciatic nerve, while the remaining 15% is responsive to inputs from the saphenous nerve. Following transection of the sciatic nerve, all hindpaw skin regions normally innervated by the sciatic nerve remained denervated. In cortex, the representation of cutaneous inputs from the saphenous nerve expanded into parts of the hindpaw region normally representing sciatic inputs and occupied an area about 3 times larger than the saphenous representation in normal rats. This expansion was initially observed 1 to 2 days after transection and was stably maintained with longer deafferentation times. However, even after chronic deafferentation of up to 5 months, this enlarged saphenous representation was still only half the size of the normal hindpaw representation in normal rats. These findings suggest that cortical representations of deafferented skin can become activated by substitute cutaneous inputs. The rapid time course for substitution suggests these changes are due to functional modifications in normally existing connections. With the deafferentation conditions used in the present study, input substitution was limited to only parts of the deprived cortex. A hypothesis is presented which suggests these changes are due to adjustments in the dominance of saphenous and sciatic inputs to specific regions of cortex.
196 citations
"Large-Scale Reorganization in the S..." refers background in this paper
...…demonstrated in a variety of mammalian species after different kinds of deprivations including digit or limb amputations (Merzenich et al., 1984; Wall and Cusick, 1984; Calford and Tweedale, 1988; Turnbull and Rasmusson, 1991; Florence et al., 1998), nerve transections (Wall and Kaas, 1985;…...
[...]
...Since then, reorganization of the cortical maps has been demonstrated in a variety of mammalian species after different kinds of deprivations including digit or limb amputations (Merzenich et al., 1984; Wall and Cusick, 1984; Calford and Tweedale, 1988; Turnbull and Rasmusson, 1991; Florence et al., 1998), nerve transections (Wall and Kaas, 1985; Garraghty and Kaas, 1991b), dorsal root transections (Pons et al....
[...]