Beyond body maps: Information content of specific body parts is distributed across the somatosensory homunculus

Muret, Dollyane; Root, Victoria; Kieliba, Paulina; Clode, Danielle; Makin, Tamar R.

doi:10.1016/j.celrep.2022.110523

Cited by 42 publications

(33 citation statements)

References 101 publications

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“…Interfinger overlap and selectivity are both important aspects of the topographic hand map, and our findings provide a nuancing contrast to net selectivity alone, which has dominated human research on deprivation-triggered plasticity. This view is consistent with a recent demonstration that the information content of body parts and sub-parts is more distributed across S1 than selectivity maps suggest ( 12 ).…”

Section: Discussionsupporting

confidence: 92%

“…Because these ripples activate mechanoreceptors on other fingers, even localized tactile stimulation elicits widely distributed peripheral responses, with distinct spatiotemporal patterns ( 8 ). Together with related findings characterizing the organizational features of the S1 hand map that are not necessarily anchored to topographic maps ( 9 – 12 ), these results suggest that shared somatosensory processing of inputs from multiple skin surfaces across the hand is more prevalent than typically appreciated.…”

Section: Introductionsupporting

confidence: 57%

“…At that level, the dominant (but not universal) interpretation of the classic work personified by Merzenich that the deprived cortex is rapidly overwritten clashes with persistent hand representation in humans. We hypothesized that this apparent contradiction may have resulted from a strong focus on selectivity as a key organizing principle in S1, at the expense of the known overlap across finger representations [see also ( 12 )]. At least in the short term, what appears to be local remapping of input to the deprived cortex does not have to be caused by the reorganization of sensory cortex.…”

Section: Introductionmentioning

confidence: 99%

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Malleability of the cortical hand map following a finger nerve block

et al. 2022

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Electrophysiological studies in monkeys show that finger amputation triggers local remapping within the deprived primary somatosensory cortex (S1). Human neuroimaging research, however, shows persistent S1 representation of the missing hand’s fingers, even decades after amputation. Here, we explore whether this apparent contradiction stems from underestimating the distributed peripheral and central representation of fingers in the hand map. Using pharmacological single-finger nerve block and 7-tesla neuroimaging, we first replicated previous accounts (electrophysiological and other) of local S1 remapping. Local blocking also triggered activity changes to nonblocked fingers across the entire hand area. Using methods exploiting interfinger representational overlap, however, we also show that the blocked finger representation remained persistent despite input loss. Computational modeling suggests that both local stability and global reorganization are driven by distributed processing underlying the topographic map, combined with homeostatic mechanisms. Our findings reveal complex interfinger representational features that play a key role in brain (re)organization, beyond (re)mapping.

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Section: Discussionsupporting

confidence: 92%

Section: Introductionsupporting

confidence: 57%

Section: Introductionmentioning

confidence: 99%

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Malleability of the cortical hand map following a finger nerve block

et al. 2022

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“…This may be related to the recent finding that different body parts are represented by distinct resting-state functional networks (Thomas et al, 2021), hence possibly also affecting oscillatory rhythms that are thought to arise from activity of neural feedback loops (Bollimunta et al, 2011;Halgren et al, 2019;van Kerkoerle et al, 2014). Second, the segregation of hand and foot areas in the primary somatosensory cortex may be less strict than commonly assumed on the basis of the somatosensory homunculus, with sometimes overlapping representations of distant body parts (Catani, 2017;Muret et al, 2022). In congruence with this account, event-related synchronization of beta band activity after toe stimulation has also been reported in hand regions in humans (in addition to foot regions; Gaetz and Cheyne, 2006) and chemogenetic silencing of hand regions in monkeys may be associated with a disinhibition of foot areas (as measured by BOLD responses using fMRI; Hirabayashi et al, 2021).…”

Section: Differences In Oscillatory State Response Dynamics Between H...mentioning

confidence: 99%

Cortical response variability is driven by local excitability changes with somatotopic organization

Stephani

Nierula

Villringer

et al. 2022

Preprint

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Identical sensory stimuli can lead to different neural responses depending on the instantaneous brain state. Specifically, neural excitability in sensory areas may shape the brain’s response already from earliest cortical processing onwards. However, whether these dynamics affect sensory domains globally or occur on a spatially local level is largely unknown. We studied this in the somatosensory domain of 38 human participants with EEG, presenting stimuli to the median and tibial nerves alternatingly, and testing the co-variation of initial cortical responses in hand and foot areas, as well as their relation to pre-stimulus oscillatory states. We found that amplitude fluctuations of initial cortical responses to hand and foot stimulation – the N20 and P40 components of the somatosensory evoked potential (SEP), respectively – were not related, indicating local excitability changes in primary sensory regions. In addition, effects of pre-stimulus alpha (8-13 Hz) and beta (18-23 Hz) band amplitude on hand-related responses showed a robust somatotopic organization, thus further strengthening the notion of local excitability fluctuations. However, for foot-related responses, the spatial specificity of pre-stimulus effects was less consistent across frequency bands, with beta appearing to be more foot-specific than alpha. Connectivity analyses in source space suggested this to be due to a somatosensory alpha rhythm that is primarily driven by activity in hand regions while beta frequencies may operate in a more hand-region-independent manner. Altogether, our findings suggest spatially distinct excitability dynamics within the primary somatosensory cortex, yet with the caveat that frequency-specific processes in one sub-region may not readily generalize to other sub-regions.

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“…Studies of the primate hand have shown that S1 neural activity contains non-linear interactions when multiple fingers are stimulated simultaneously [48], [50], supporting the idea that S1 carries information beyond a linear report of inputs from tactile receptors. In humans, S1 has recently been shown to represent body parts outside of their traditionally defined areas [51], [52].…”

Section: Introductionmentioning

confidence: 99%

S1 represents multisensory contexts and somatotopic locations within and outside the bounds of the cortical homunculus

Rosenthal

Bashford

Kellis

et al. 2022

Preprint

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The responsiveness of primary somatosensory cortex (S1) to physical tactile stimuli is well documented but the extent to which it is modulated by vision is unresolved. Additionally, recent literature has suggested that tactile events are represented in S1 in a more complex, generalized manner than its long-established topographic organization. To better characterize S1 function, neural activity was recorded from a tetraplegic patient implanted with microelectrode arrays in S1 during 1s stroking touches to the forearm (evoking numb sensation) or finger (naturalistic sensation). Touch conditions included visually observed first person physical touches, physical touches without vision, and visual touches without physical contact which occurred either to a third person, an inanimate object, or the patient's own body in virtual reality. Two major findings emerged from this dataset. The first was that vision strongly modulates S1 activity, but only if there is a physical element to the touch, suggesting that passive observation of touches is not sufficient to recruit S1 neurons. The second was that despite the location of the recording arrays in a putative arm area of S1, neural activity was able to represent both arm and finger touches in physical touch conditions. Arm touches were encoded more strongly and specifically, supporting the idea that S1 encodes tactile events primarily through its topographic organization, as well as in a more general manner encompassing larger areas of the body.

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Beyond body maps: Information content of specific body parts is distributed across the somatosensory homunculus

Cited by 42 publications

References 101 publications

Malleability of the cortical hand map following a finger nerve block

Malleability of the cortical hand map following a finger nerve block

Cortical response variability is driven by local excitability changes with somatotopic organization

S1 represents multisensory contexts and somatotopic locations within and outside the bounds of the cortical homunculus

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