Stability of Sensory Topographies in Adult Cortex

doi:10.1016/j.tics.2017.01.002

Trends in Cognitive Sciences

Volume 21, Issue 3, March 2017, Pages 195-204

https://doi.org/10.1016/j.tics.2017.01.002 Get rights and content

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The reorganisation of primary somatosensory cortex (SI) following arm amputation is considered a prime example of neural plasticity in the adult brain and of its consequences on altered perception.

Recent evidence from human and non-human primates shows that the reorganisation in SI does not result in novel functional sensory representations and that somatotopic organisation persists despite drastic loss of sensory input.

Perceptual reports from human subjects suggest that the loss of sensory input does not result in a replacement of the original representation: activation of the missing hand area evokes sensations referred to the missing (phantom) hand and not to the ‘invading’ body regions (e.g., the face).

The evidence for preserved somatotopy following long-term deafferentation has important implications for providing artificial touch through electrical interfaces with the nervous system.

Textbooks teach us that the removal of sensory input to sensory cortex, for example, following arm amputation, results in massive reorganisation in the adult brain. In this opinion article, we critically examine evidence for functional reorganisation of sensory cortical representations, focusing on the sequelae of arm amputation on somatosensory topographies. Based on literature from human and non-human primates, we conclude that the cortical representation of the limb remains remarkably stable despite the loss of its main peripheral input. Furthermore, the purportedly massive reorganisation results primarily from the formation or potentiation of new pathways in subcortical structures and does not produce novel functional sensory representations. We discuss the implications of the stability of sensory representations on the development of upper-limb neuroprostheses.

Section snippets

Plasticity in Sensory Cortical Topographies

One of the key concepts in contemporary neuroscience is that experience shapes the central nervous system throughout life. The ability of the brain to adaptively change how it processes inputs based on new experience is termed ‘plasticity’ and underlies our ability to mature, learn new skills, and recover from injury. Our current understanding of neuroplasticity has been moulded by the work of Hubel and Wiesel 1, 2, 3 in the 1960s, who studied the visual cortex of cats following temporary

Functional Benefits of Reorganisation?

If deafferented cortex begins to process a new patch of the sensory sheet (on the retina or the skin), one would expect that the additional cortical volume would lead to perceptual gains for this ‘invading’ region (i.e., adaptive plasticity, see 14, 15). For example, SI remapping following digit amputation results in increased representation of the neighbouring digits, which in turn should lead to increased acuity for these digits [8]. Such perceptual gains would imply that signals arising to

Phantom and Referred Sensations

If remapping in SI does not result in direct perceptual gains, are there any other functional consequences to SI remapping? In other words, are these invading signals behaviourally relevant? The most extensively documented and captivating consequence relates to distorted phantom sensations following amputation. Even decades after injury, amputees report a continued sensation of the limb that is no longer there. These phantom sensations can be as vivid and as natural as the perception of one’s

Reorganisation in Humans

Results from neuroimaging studies in human amputees further challenge the view that neighbouring cortical representations invade the deafferented ones. While the lip representation encroaches somewhat on the limb representation following amputation, it does not annex it completely 36, 37, 38 in contrast to what is observed in electrophysiological recordings from amputated or deafferented monkeys 11, 12. Rather, the deafferented territory in human somatosensory cortex begins to respond to body

Persistent Representation Despite Input Loss

A further challenge to the notion that reorganisation causes functional consequences is provided by the perceptual correlates of nerve stimulation. Numerous studies have shown that, when the residual (injured) nerve is electrically stimulated, either directly 41, 42 or transcutaneously 43, 44, individuals experience the evoked somatosensory percepts as vividly and clearly arising from their phantom hand (Figure 2C), and not from other body parts such as the face. In fact, stimulation of the

Neural Basis of Reorganisation

The persistence of sensory experience despite peripheral input loss can be explained in part by nerve regeneration. Indeed, a severed sensory axon typically regrows and spontaneously reinnervates intact skin, for example, on the residual arm (see [47] for physiological review). As a result, touch applied to the reinnervated skin will produce signals that are mislabelled by the central nervous system as arising from the missing hand and result in a sensation projected to the missing hand. As

Stability of Sensory Topographies in Adult Cortex

In summary, loss of input from a body region in adulthood leads to the formation or potentiation of lateral connections in the brainstem, which gives rise to a new pathway from periphery to cortex. This new pathway alone can account for the face-elicited activity in monkeys’ hand cortex, and the contribution of cortical reorganisation per se remains unconfirmed. The original pathway seems to be relatively spared as evidenced by the elicitation of sensations evoked on the amputated or insensate

Neural Basis of Stable Cortical Representations

The stability of sensory topographies may be attributable to at least two factors. First, to form a new sensory representation requires reorganisation spanning a wide swath of cortex over which the representation is distributed in a functionally organised way, and the mechanisms of plasticity may not operate on sufficiently large spatial scales in the nervous system to allow for this. In fact, sensory topographies have been shown to be in part determined by genetically controlled patterning

Concluding Remarks and Future Perspectives for Brain Machine Interfaces

The aforementioned reinterpretation of the behavioural, imaging, and neurophysiological results implies a more nuanced view of cortical plasticity: while sensory cortices of adults are endowed with plasticity, this plasticity cannot result in the formation of completely novel representations, even under the extreme circumstance of deafferentation. To establish that aberrant activity in deprived cortex constitutes a new sensory representation of the displaced input requires causal evidence, for

Acknowledgements

The authors thank Jon Kaas, Murray Sherman, Jeffrey Yau, Patrick Haggard, and Jeremy Winberry for helpful comments on a previous version of this manuscript. T.R.M. was supported by a Henry Dale Fellowship jointly funded by the Wellcome Trust and the Royal Society (Grant No. 104128/Z/14/Z). S.J.B. was supported by NINDS grantsR01 NS095251 and NS 095162.

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Cited by (87)

Reassessing referral of touch following peripheral deafferentation: The role of contextual bias
2023, Cortex
Some amputees have been famously reported to perceive facial touch as arising from their phantom hand. These referred sensations have since been replicated across multiple neurological disorders and were classically interpreted as a perceptual correlate of cortical plasticity. Common to all these and related studies is that participants might have been influenced in their self-reports by the experimental design or related contextual biases. Here, we investigated whether referred sensations reports might be confounded by demand characteristics (e.g., compliance, expectation, suggestion). Unilateral upper-limb amputees (N = 18), congenital one-handers (N = 19), and two-handers (N = 22) were repeatedly stimulated with computer-controlled vibrations on 10 body-parts and asked to report the occurrence of any concurrent sensations on their hand(s). To further manipulate expectations, we gave participants the suggestion that some of these vibrations had a higher probability to evoke referred sensations. We also assessed similarity between (phantom) hand and face representation in primary somatosensory cortex (S1), using functional Magnetic Resonance Imaging (fMRI) multivariate representational similarity analysis. We replicated robust reports of referred sensations in amputees towards their phantom hand; however, the frequency and distribution of reported referred sensations were similar across groups. Moreover, referred sensations were evoked by stimulation of multiple body-parts and similarly reported on both the intact and phantom hand in amputees. Face-to-phantom-hand representational similarity was not different in amputees' missing hand region, compared with controls. These findings weaken the interpretation of referred sensations as a perceptual correlate of S1 plasticity and reveal the need to account for contextual biases when evaluating anomalous perceptual phenomena.
Layer-specific vulnerability is a mechanism of topographic map aging
2023, Neurobiology of Aging
Topographic maps form a critical feature of cortical organization, yet are poorly described with respect to their microstructure in the living aging brain. We acquired quantitative structural and functional 7T-MRI data from younger and older adults to characterize layer-wise topographic maps of the primary motor cortex (M1). Using parcellation-inspired techniques, we show that quantitative T1 and Quantitative Susceptibility Maps values of the hand, face, and foot areas differ significantly, revealing microstructurally distinct cortical fields in M1. We show that these fields are distinct in older adults and that myelin borders between them do not degenerate. We further show that the output layer 5 of M1 shows a particular vulnerability to age-related increased iron, while layer 5 and the superficial layer show increased diamagnetic substance, likely reflecting calcifications. Taken together, we provide a novel 3D model of M1 microstructure, where body parts form distinct structural units, but layers show specific vulnerability toward increased iron and calcium in older adults. Our findings have implications for understanding sensorimotor organization and aging, in addition to topographic disease spread.
S1 represents multisensory contexts and somatotopic locations within and outside the bounds of the cortical homunculus
2023, Cell Reports
Recent literature suggests that tactile events are represented in the primary somatosensory cortex (S1) beyond its long-established topography; in addition, the extent to which S1 is modulated by vision remains unclear. To better characterize S1, human electrophysiological data were recorded during touches to the forearm or finger. Conditions included visually observed physical touches, physical touches without vision, and visual touches without physical contact. Two major findings emerge from this dataset. First, vision strongly modulates S1 area 1, but only if there is a physical element to the touch, suggesting that passive touch observation is insufficient to elicit neural responses. Second, despite recording in a putative arm area of S1, neural activity represents both arm and finger stimuli during physical touches. Arm touches are encoded more strongly and specifically, supporting the idea that S1 encodes tactile events primarily through its topographic organization but also more generally, encompassing other areas of the body.
Multifaceted understanding of human nerve implants to design optimized electrodes for bioelectronics
2022, Biomaterials
Citation Excerpt :
Our results suggest that the perception changes observed during the trial were caused by the peripheral nerve reactions to the implanted electrodes more than a major effect of the neuroprosthetic use inducing a brain plasticity and remap [53]. This is in line with findings on the high stability of the cortical sensory map in adulthood and their impossibility to be modified, even with prolonged exposure [54]. Moreover, the variation in the perceptual thresholds was also observed with Utah electrodes used for ICMS (intracortical micro-stimulation) for sensory feedback restoration in humans [55].
Bioelectronic medicine is a promising venue for treatment of disabilities using implantable neural interfaces. Peripheral neurostimulation of residual nerves recently enabled multiple functional benefits in amputees. Despite the preliminary promising impact on patients' life, the over-time stability of implants and the related nerve reactions are unclear. To unveil the mechanisms and inform the design of better nerve-electrode interfaces, we engaged a multifaceted approach, merging functional responses from patients, their histological data, and corresponding computational modelling. Neurostimulation evoked different selective sensation locations and qualities over-time, with respective perceptual thresholds, that showed different degree of time stabilities dependent from the stimulating active sites. The histological analysis after explant showed mild tissue reactions, while electromechanically active sites and substrates remained conserved. Computational models, based on patients' histology, revealed the direct influence of the simulated tissue reaction to change of thresholds and type of perceived sensations. Novel insights of electrode biocompatibility was observed compared to animals and the increase of thresholds could be predicted computationally. This multifaced framework suggest that future intraneural implants should have easier implantation and higher biocompatibility counteracting the sensations changes through AI-based stimulations and electrode coatings.
Clinical neuroscience and neurotechnology: An amazing symbiosis
2022, iScience
In the last decades, clinical neuroscience found a novel ally in neurotechnologies, devices able to record and stimulate electrical activity in the nervous system. These technologies improved the ability to diagnose and treat neural disorders. Neurotechnologies are concurrently enabling a deeper understanding of healthy and pathological dynamics of the nervous system through stimulation and recordings during brain implants. On the other hand, clinical neurosciences are not only driving neuroengineering toward the most relevant clinical issues, but are also shaping the neurotechnologies thanks to clinical advancements. For instance, understanding the etiology of a disease informs the location of a therapeutic stimulation, but also the way stimulation patterns should be designed to be more effective/naturalistic. Here, we describe cases of fruitful integration such as Deep Brain Stimulation and cortical interfaces to highlight how this symbiosis between clinical neuroscience and neurotechnology is closer to a novel integrated framework than to a simple interdisciplinary interaction.
Preserved cortical somatotopic and motor representations in tetraplegic humans
2022, Current Opinion in Neurobiology
A rich literature has documented changes in cortical representations of the body in somatosensory and motor cortex. Recent clinical studies of brain–machine interfaces designed to assist paralyzed patients have afforded the opportunity to record from and stimulate human somatosensory, motor, and action-related areas of the posterior parietal cortex. These studies show considerable preserved structure in the cortical somato-motor system. Motor cortex can immediately control assistive devices, stimulation of somatosensory cortex produces sensations in an orderly somatotopic map, and the posterior parietal cortex shows a high-dimensional representation of cognitive action variables. These results are strikingly similar to what would be expected in a healthy subject, demonstrating considerable stability of adult cortex even after severe injury and despite potential plasticity-induced new activations within the same region of cortex. Clinically, these results emphasize the importance of targeting cortical areas for BMI control signals that are consistent with their normal functional role.

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Trends in Cognitive Sciences

OpinionStability of Sensory Topographies in Adult Cortex

Trends

Section snippets

Plasticity in Sensory Cortical Topographies

Functional Benefits of Reorganisation?

Phantom and Referred Sensations

Reorganisation in Humans

Persistent Representation Despite Input Loss

Neural Basis of Reorganisation

Stability of Sensory Topographies in Adult Cortex

Neural Basis of Stable Cortical Representations

Concluding Remarks and Future Perspectives for Brain Machine Interfaces

Acknowledgements

J. Hand Ther.

Exp. Neurol.

Prog. Brain Res.

Neurosci. Lett.

NeuroImage

J. Hand Surg. Am.

Pain

Curr. Biol.

Curr. Biol.

Trends Cogn. Sci. (Regul. Ed.)

Neurosci. Biobehav. Rev.

Binocular interaction in striate cortex of kittens reared with artificial squint

J. Neurophysiol.

Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens

J. Neurophysiol.

Extent of recovery from the effects of visual deprivation in kittens

J. Neurophysiol.

Lack of long-term cortical reorganization after macaque retinal lesions

Nature

Large-scale remapping of visual cortex is absent in adult humans with macular degeneration

Nat. Neurosci.

Plasticity, and its limits, in adult human primary visual cortex

Multisens. Res.

Multiple representations of the body within the primary somatosensory cortex of primates

Science

Somatosensory cortical map changes following digit amputation in adult monkeys

J. Comp. Neurol.

Map plasticity in somatosensory cortex

Science

Massive cortical reorganization after sensory deafferentation in adult macaques

Science

Large-scale reorganization in the somatosensory cortex and thalamus after sensory loss in macaque monkeys

J. Neurosci.

Neural reorganization following sensory loss: the opportunity of change

Nat. Rev. Neurosci.

Spatial acuity after digit amputation

Brain

Reorganization of sensory function in amputation stumps: two-point discrimination

Fed. Proc.

Reactions to loss of limb: physiological and psychological aspects

Ann. N. Y. Acad. Sci.

Deafferentation of the affected arm: a method to improve rehabilitation?

Stroke

Enhanced tactile spatial acuity and cortical processing during acute hand deafferentation

Nat. Neurosci.

Tactile perception in blind Braille readers: a psychophysical study of acuity and hyperacuity using gratings and dot patterns

Percept. Psychophys.

The use of visual feedback, in particular mirror visual feedback, in restoring brain function

Brain

Behavioral and magnetoencephalographic correlates of plasticity in the adult human brain

Proc. Natl. Acad. Sci. U. S. A.

Perceptual correlates of massive cortical reorganization

Neuroreport

Thumb in cheek? Sensory reorganization and perceptual plasticity after limb amputation

Neuroreport

Sensory disorganization and perceptual plasticity after limb amputation: a follow-up study

Neuroreport

Large-scale sprouting of cortical connections after peripheral injury in adult macaque monkeys

Science

Thalamic and brainstem contributions to large-scale plasticity of primate somatosensory cortex

Science

Opinion
Stability of Sensory Topographies in Adult Cortex