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: In this paper, five macaque monkeys received months of enriched sensory experience after median nerve cut and repair early in life, and the most substantial effect of the sensory environment was on receptive field sizes in cortical area 3b.
Abstract: Sensory perception can be severely degraded after peripheral injuries that disrupt the functional organization of the sensory maps in somatosensory cortex, even after nerve regeneration has occurred. Rehabilitation involving sensory retraining can improve perceptual function, presumably through plasticity mechanisms in the somatosensory processing network. However, virtually nothing is known about the effects of rehabilitation strategies on brain organization, or where the effects are mediated. In this study, five macaque monkeys received months of enriched sensory experience after median nerve cut and repair early in life. Subsequently, the sensory representation of the hand in primary somatosensory cortex was mapped using multiunit microelectrodes. Additionally, the primary somatosensory relay in the thalamus, the ventroposterior nucleus, was studied to determine whether the effects of the enrichment were initiated subcortically or cortically. Age-matched controls included six monkeys with no sensory manipulation after median nerve cut and regeneration, and one monkey that had restricted sensory experience after the injury. The most substantial effect of the sensory environment was on receptive field sizes in cortical area 3b. Significantly greater proportions of cortical receptive fields in the enriched monkeys were small and well localized compared to the controls, which showed higher proportions of abnormally large or disorganized fields. The refinements in receptive field size and extent in somatosensory cortex likely provide better resolution in the sensory map and may explain the improved functional outcomes after rehabilitation in humans.
45 citations
"Large-Scale Reorganization in the S..." refers background 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 level by complex interactions of the divergent feedforward and feedback connections (Ergenzinger et al....
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...…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 by complex interactions of the divergent feedforward…...
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TL;DR: The Telescoping perception of a phantom limb by the stimulation of misallocation points was correlated with lenticular nuclei, thalamic and cingulate gyrus activation, and the involvement of subcortical structures in phantom limb telescoping perception was examined.
29 citations
"Large-Scale Reorganization in the S..." refers background in this paper
...In another study, in the post central cortex, a larger than normal activation was seen on stimulation of the stump in a person with lower leg amputation (Condés-Lara et al., 2000)....
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...In another study, in the post central cortex, a larger than normal activation was seen on stimulation of the stump in a person with lower leg amputation (Condés-Lara et al., 2000)....
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TL;DR: Multiunit recordings along mediolateral rows in the primary somatosensory cortex of the animals described by C. Avendafio and D. Umbriaco provided information about the functional status of the regions in and near the deafferented cortex.
Abstract: Multiunit recordings along mediolateral rows in the primary somatosensory cortex of the animals described by C. Avendano, D. Umbriaco, R.W. Dykes, and L. Descarries (1995, J. Comp. Neurol. 354:321-332) provided information about the functional status of the regions in and near the deafferented cortex. Responses changed along this axis from normally organized receptive fields in the hindlimb representation through a transition zone of unusually small receptive fields into the clearly deafferented forelimb representation, where receptive fields were uncommon and often had unusual characteristics. The most abrupt change along this axis was the appearance of a repetitive, bursting discharge pattern in the multiunit activity near the border of the deprived cortex. The appearance of this pattern was used as a reference to describe differences between normal and deprived cortices. The nature of these differences evolved with time. Much of the deprived cortex lacked identifiable receptive fields for months after the nerve transections and, 1 year later, still only about half of the recording sites within the deprived region displayed organized receptive fields. Some sites within the deprived region lacking definable receptive fields could be excited at long latencies by somatic stimuli anywhere on the body. With time, regions of normal cortex near the border with the deprived zone became more involved in these processes. Spontaneous activity and thresholds also changed with time in both normal and deprived cortices.(ABSTRACT TRUNCATED AT 250 WORDS)
28 citations
"Large-Scale Reorganization in the S..." refers background in this paper
...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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7 citations
"Large-Scale Reorganization in the S..." refers background in this paper
...Adult brains retain a remarkable ability to change in response to injuries that interrupt transmission of peripheral inputs resulting from damage to the peripheral or central pathways (Jones, 2000; Chen et al., 2002; Jain, 2002; Kaas et al., 2008)....
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