The homeostatic homunculus: rethinking deprivation-triggered reorganisation
Section snippets
Balancing between plasticity and stability
Seminal work on sensorimotor plasticity has established the notion that the adult cortex is extremely plastic. For example, following amputation of a finger [1] or deafferentation of an arm [2], the deprived primary somatosensory cortex (SI) of monkeys becomes activated by inputs of the cortically neighbouring finger or face, resulting in shifted map boundaries. It has long been assumed that such cortical remapping has direct consequences on perception and action, for example in the context of
Persistent representation despite cortical remapping
Contrary to the prevalent view of cortical remapping but consistent with the concept of homeostasis, recent accumulating evidence demonstrates that the canonical representational structure and function of the deprived cortex persist after amputation. This research draws on the lingering sensations arising from the missing limb that affect up to 90% of adult upper-limb amputees [15]. By taking advantage of amputees’ ability to voluntarily move their phantom hand, the signals elicited both
Cortical remapping despite persistent representation
How can we resolve the classical notion of remapping with this newly accumulating evidence for persistent representation? While these two processes are intuitively contradictory, it is important to point that they are not mutually exclusive, and can in fact co-exist [17,18,24]. Here we suggest that in the context of the brain’s need for homeostasis, these processes are more complementary, in particular when considering the functional organisation of the sensorimotor cortex.
Following on
Considering activity-dependent plasticity as a stabilising principle
Plasticity in the adult sensorimotor cortex following deprivation has also been suggested to be triggered by contextual changes to the spared input, due to adaptive behaviour. For instance, unilateral arm amputees increasingly rely on their intact hand for daily functioning, and this over use could relate to increased activity for the intact hand in amputees’ (ipsilateral) deprived hand area, resulting in remapping of the intact hand’s activity profile [40, 41, 42]. In the context of
Activity-dependent plasticity in early development brings a new perspective to homunculus organisation and remapping
While large-scale SI reorganisation might be more limited in adults than originally considered, early life development offers a more favourable environment for activity-dependent plasticity. This is because brain organisation is particularly sensitive to experience and activity during a critical period within development [44], and because white matter pathways are still under determined (e.g. pruning). Additionally, homeostatic principles may be different for a developing brain and allow for
Concluding remarks
Here we offer a new perspective on the literature of deprivation-triggered sensorimotor plasticity, by emphasising the brain’s need for homeostasis and the presence of distributed latent activity across the homunculus. We suggest that these two guiding principles can unify disparate, and often intuitively contradictory evidence, relating to the sensorimotor system’s response to deprivation following amputation. Persistent missing-hand representation and activity-dependent plasticity may both
Conflict of interest statement
Nothing declared.
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
This work was supported by an ERC Starting Grant (715022 EmbodiedTech) and a Wellcome Trust Senior Research Fellowship (215575/Z/19/Z), awarded to TRM. We thank Avital Hahamy, Daan Wesselink, Hannes Saal, Ella Striem-Amit and Esther Kuehn for helpful feedback on the manuscript and Arabella Bouzigues for proof reading.
Glossary
- Homeostasis
- Mechanisms that can either strengthen or weaken activity that is respectively above or below what is necessary to maintain baseline function and activity balance at either a local or a network level.
- Remapping
- Changes to cortical map boundaries or topography, quantified based on activity measures. For example, activity for one body-part identified in the cortical area of another body-part.
- Reorganisation
- Activity changes that introduce new local representational content and readout to
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Response to: Letter to the Editor on “Failure to Compensate: Patients With Nerve Injury Use Their Injured Dominant Hand, Even When Their Nondominant is More Dexterous”
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2023, Neuroscience and Biobehavioral ReviewsBeyond body maps: Information content of specific body parts is distributed across the somatosensory homunculus
2022, Cell ReportsCitation Excerpt :Due to its highly selective profile, conventional mapping procedures providing a “parcellated”—all or nothing (i.e., winner takes all)—view over S1 have dominated our conceptualization of its functional organization (Roux et al., 2018; Willoughby et al., 2021). Consequently, alteration of map boundaries have been commonly interpreted as cortical reorganization, with the limitations previously discussed (Muret and Makin, 2021). Using conventional univariate analyses, together with multivariate RSA, we investigated the distribution of information content underlying S1 topographic organization.
The various forms of sensorimotor plasticity following limb amputation and their link with rehabilitation strategies
2021, Revue NeurologiqueCitation Excerpt :Their results further yielded to a similar underlying mechanism, driven by an abnormally enhanced spontaneous activity of deafferented nociceptive channels, driven by a deafferentation-related disinhibition [55]. Muret and Makin lately suggested that if deprivation triggers remapping of the adjacent body parts through the unmasking of pre-existing latent activity, it might correspond to a latent form of activity along the homunculus, which in turn, elicits homeostatic regulations through the maintenance of the persistent representation of a missing hand [56]. They further suggest that since the activity of the latent connections was already present, remapping could somehow correspond to functional stability of the sensorimotor system rather than reorganisation.
Representation and perception of the body in space
2021, Encyclopedia of Behavioral Neuroscience: Second Edition