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 suggest that the release of inhibitory responses in a cortical digital region by amputation is prevented by the retention of even one ventral nerve.
Abstract: The immediate effects of total or partial denervation of single digits (0-16 hr after nerve transection) on primary somatosensory cortex were studied electrophysiologically. Comparisons of response properties and cortical somatotopy were made between intact raccoons and four groups of raccoons with transection of some or all of the nerves innervating the fourth or fifth digit. Animals with all four digital nerves cut (amputation of the digit) were most different from normal. Approximately half of the penetrations in the affected cortical region showed inhibitory responses to stimulation of adjacent skin regions. These consisted of a strong response to stimulus offset and/or a suppression of spontaneous activity during indentation. Since these responses were substantially different from those recorded several months after digit amputation, additional changes in connectivity and synaptic strength must occur with chronic denervation. These inhibitory responses were not seen in animals with one, two, or three nerves cut per digit. In the animals with partial denervation of a digit, the greatest disruption occurred when both ventral nerves to the glabrous skin were transected. This yielded cell clusters with abnormally large receptive fields, disruptions in somatotopic organization, and a decreased occurrence of low-threshold responses. If only one nerve to glabrous skin was transected, there was less change, even if it was combined with transection of both nerves to hairy skin. These results suggest that the release of inhibitory responses in a cortical digital region by amputation is prevented by the retention of even one ventral nerve. None of the denervation conditions produced large nonresponsive areas of cortex, which would have indicated a loss of all inputs.
70 citations
TL;DR: The results and the literature reviewed suggest that the cutaneous region served by one spinal nerve is actually much wider and much more variable in location than is generally recognized.
Abstract: Single fibres were dissected from the dorsal spinal roots of the nerves serving the brachial plexus in African green monkeys. The dermatomal organization of these spinal nerves was deduced from data concerning the receptive fields of 2834 single afferent fibres. These data were collected in an attempt to reconcile some of the discrepancies that exist in published descriptions of the dermatomes in primates; our results and the literature reviewed suggest that the cutaneous region served by one spinal nerve is actually much wider and much more variable in location than is generally recognized. This makes any summary diagram a misleading indicator of the true complexity of the spinal innervation of the upper limb. In spite of this variability among individuals, within any specific individual there is a regular and orderly progression of innervation which allows prediction of the region served by a particular spinal nerve when information concerning the site of innervation of adjacent nerves is available. The territory of each myotome tended to be larger than the dermatome of the same spinal nerve. Most muscles of the limb received afferent innervation from three to four different spinal nerves. Further, the territory of the myotome did not of necessity coincide with the dermatome of the same spinal nerve. Even those nerves innervating the hand still innervated axial muscles. These observations have important implications for the diagnosis of spinal nerve injuries.
70 citations
"Large-Scale Reorganization in the S..." refers background or methods 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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...The receptive fields on the arm were found on the anterior upper arm and radial forearm for which inputs enter the spinal cord rostral to the level of the lesion at C6/C7 (Sherrington, 1939; Dykes and Terzis, 1981)....
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TL;DR: 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.
Abstract: 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. © 1996 Wiley-Liss, Inc.
69 citations
"Large-Scale Reorganization in the S..." refers background in this paper
..., 2004), or immediately after median and radial nerve injury or block (Silva et al., 1996; Weiss et al., 2004)....
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TL;DR: The data imply that the recovery of precision grip using the thumb and index finger depends on the survival of afferents innervating these digits, as well as the proliferation of their central terminals.
Abstract: The recovery of manual dexterity was analyzed in the macaque following a cervical dorsal root section that abolished cutaneous feedback from selected digits of one hand. Monkeys were trained to retrieve a target object from a clamp using thumb and index finger opposition. Dorsal rootlets containing electrophysiologically identified axons projecting from the thumb and index finger were then cut in two monkeys (Group 1). In four others (Group 2), additional rootlets shown to innervate the middle finger and thenar eminence were also transected. Three performance parameters were analyzed before and following the rhizotomy: 1) percentage of successful retrievals; 2) digital stratagem (the pattern of digit opposition); and 3) contact time (duration of digit contact with the object before its retrieval). During the first postoperative week, hand function was severely impaired in all monkeys. Over the following weeks, Group 1 monkeys recovered the ability to retrieve the object by opposing the index finger and thumb in >80% of trials. Group 2 monkeys also regained some function in the impaired hand: each monkey adopted a stratagem for grasping the target, using digits that were incompletely deafferented. In the terminal experiment, hand representation in the contralateral somatosensory cortex was electrophysiologically mapped to define hand deafferentation and cortical reactivation further. There was a close correspondence between the cortical map and digit use. Our data imply that the recovery of precision grip using the thumb and index finger depends on the survival of afferents innervating these digits, as well as the proliferation of their central terminals. J. Comp. Neurol. 491:27–45, 2005. © 2005 Wiley-Liss, Inc.
68 citations
"Large-Scale Reorganization in the S..." refers background in this paper
...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 results demonstrate peripherally mediated central reorganization in young adult macaque monkeys by selectively removing cutaneous input from the index finger and thumb by lesioning dorsal rootlets to examine both immediate and long-term systemic responses to this deficit.
Abstract: Chronic peripheral nerve injuries produce neural changes at different levels of the somatosensory pathway, but these responses remain poorly defined. We selectively removed cutaneous input from the index finger and thumb in young adult macaque monkeys by lesioning dorsal rootlets to examine both immediate and long-term systemic responses to this deficit. Corresponding digit representations within somatosensory cortex (SI) were initially silenced, but two to seven months later again responded to cutaneous stimulation of the 'deafferented' digits. We remapped cutaneous receptive fields (RFs) within adjacent intact dorsal rootlets two to four months after lesioning. RF distributions had greatly expanded, so that rootlets previously innervating adjacent hand regions now responded to stimulation of the index finger and/or thumb. Thus our results demonstrate peripherally mediated central reorganization.
64 citations
"Large-Scale Reorganization in the S..." refers background in this paper
..., 1998), nerve transections (Wall and Kaas, 1985; Garraghty and Kaas, 1991b), dorsal root transections (Pons et al., 1991; Darian-Smith and Brown, 2000), and spinal cord injuries (Jain et al....
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...…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., 1991; Darian-Smith and Brown, 2000), and spinal cord injuries (Jain et al., 1997, 2000)....
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