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.
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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)....
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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.,…...
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References
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TL;DR: The results show a lack of collateral thalamocortical projections to the fields of the postcentral gyrus and imply the independent relay of modality specific information through the thalamus.
Abstract: Retrograde axoplasmic transport of differently colored fluorescent dyes was used to determine the distributions and relative proportions of cells in the ventrobasal complex of the monkey thalamus that project to each of the architectonic fields of the first somatic sensory cortex. Fast Blue was injected into portions of area 3a identified by first recording short latency, multiunit responses to electrical stimulation of Group I afferents in a muscle nerve of the forelimb or hindlimb. Nuclear Yellow was later injected into a part of area 2 responding to maximal electrical stimulation of the same nerve. In experiments that served as controls, Fast Blue was injected into area 3b and Nuclear Yellow into area 1. The results confirm the division of the ventrobasal complex into: (i) a central core with an inner part projecting to area 3b and a surrounding part projecting to area 1; (ii) a peripheral shell projecting to areas 3a and 2 (Jones et al. 1982). A far greater proportion of VB cells projects to areas 3b or 3a than to areas 1 or 2. In portions of the ventrobasal complex projecting to two areas, no cells were double labelled provided that the injections of blue and yellow dyes did not overlap. The results, thus, show a lack of collateral thalamocortical projections to the fields of the postcentral gyrus and, when taken in conjunction with other data, imply the independent relay of modality specific information through the thalamus.
63 citations
"Large-Scale Reorganization in the S..." refers result in this paper
...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., 2001), which could be because of shaping of the receptive fields at each…...
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TL;DR: The somatotopic patterns of terminations in the spinal cord and cuneate nucleus of afferents from the digits of macaque monkeys were determined by the transganglionic transport of a mixture of wheat germ agglutinin conjugated with horseradish peroxidase (WGA-HRP).
63 citations
"Large-Scale Reorganization in the S..." refers background in this paper
...The sparing of the radial hand inputs corresponds to the level of the lesion as these inputs enter the spinal cord rostral to C7 (Sherrington, 1939; Florence et al., 1988, 1989)....
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...This resulted in complete sparing of inputs from the radial hand and arm and some from the ulnar hand (Sherrington, 1939; Dykes and Terzis, 1981; Florence et al., 1988, 1989; Dykes et al., 1995)....
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...A lesion at this level is expected to remove most of the inputs from digits 3, 4, and 5, while preserving those from most of the palm, digits 1 and 2 and the anterior arm (Sherrington, 1939; Florence et al., 1988; Flor et al., 1997; Darian-Smith and Ciferri, 2005)....
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TL;DR: The reactivation of hand cortex by face stimulation does not depend on a previously existing network of intrinsic cortical connections across the hand‐face border, or mismatched thalamocortical projections.
Abstract: After long-standing loss of afferents from the hand, the hand representation in area 3b of the somatosensory cortex of monkeys becomes responsive to touch on the face. Because the reactivation of deprived hand cortex by the face inputs could depend on axonal connections across the hand-face border, we determined the extent of such connections in New World marmosets, owl monkeys, and squirrel monkeys. Small injections of anatomic tracers were placed in the hand or the face representations after these representations were identified by microelectrode recordings. The positions of retrogradely labeled neurons were plotted in processed brain sections cut parallel to the brain surface, and their locations were related to anatomic isomorphs of the hand and face representations revealed in adjacent brain sections stained for myelin. In these sections, the hand-face border was clearly visualized as a myelin-poor septum. The intrinsic connections of area 3b labeled by injections in either the hand or face representations were almost completely confined to their respective representation, and very few neurons projected across the border. In addition, neurons in the somatosensory thalamus labeled by injections in either face or hand representations were confined to either VPM, representing the face, or the hand subnucleus of VPL. Thus the reactivation of hand cortex by face stimulation does not depend on a previously existing network of intrinsic cortical connections across the hand-face border, or mismatched thalamocortical projections.
61 citations
TL;DR: The results suggested an expansion of the representation of the proximal limb into the thalamic region that used to represent the amputated part, and in those patients that had a phantom limb, microstimulation in this region induced sensations perceived as originating on the phantom.
Abstract: This paper describes studies on plasticity that the author undertook with Patrick Wall in the mid '70s, and then reviews recent related studies in humans carried out in the author's laboratory. The human studies have shown that thalamic neurons frequently have subliminal receptive fields (RFs) and immediately following a reversible block of afferent activity from the RF some neurons develop increased sensitivity to tactile stimulation at sites outside their normal RF. Also described and discussed are novel findings in patients that had a limb amputated. The results suggested an expansion of the representation of the proximal limb into the thalamic region that used to represent the amputated part. Furthermore, in those patients that had a phantom limb, microstimulation in this region induced sensations perceived as originating on the phantom.
57 citations
"Large-Scale Reorganization in the S..." refers background in this paper
...The ventroposterior (VP) nucleus, the main somatosensory thalamic nucleus, also reorganizes after nerve injuries and limb amputation in monkeys and humans (Garraghty and Kaas, 1991b; Lenz et al., 1998; Dostrovsky, 1999; Florence et al., 2000)....
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TL;DR: The results suggest that these isomorphs of digits emerge in prenatal or early postnatal development and typical variations in postnatal hand use have little impact on subsequent development.
Abstract: Brain sections cut parallel to the cortical surface revealed myelin-light septa that isolated representations of the digits and parts of the face, teeth, and tongue in area 3b of adult and infant macaque monkeys The widths of the bands of cortex representing individual digits, as measured by the distances between isolating septa, were proportionally similar in infant (2–4 week) and adult monkeys However, the bands for digits 1–3 were somewhat narrower in infant than adult monkeys There was little variation in absolute widths across individuals in the infant or adult groups, or between left and right hemispheres of the same group Widths for digits 1–4 progressively decreased The results suggest that these isomorphs of digits emerge in prenatal or early postnatal development and typical variations in postnatal hand use have little impact on subsequent development As the hand representation in somatosensory cortex of monkeys may be significantly altered after the partial loss of peripheral nerve inputs, the physiological representation is not completely constrained by the isolating septa Instead, the septa may serve as a persistent marker of normal organization in studies of cortical reorganization J Comp Neurol 477:172–187, 2004 © 2004 Wiley-Liss, Inc
52 citations
"Large-Scale Reorganization in the S..." refers background in this paper
...The border between the hand and the face representations, as well as borders between the digit representations, can be visualized in histological sections of the flattened cortex stained for myelin (Jain et al., 1998, 2001; Qi and Kaas, 2004)....
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