Elsevier

Current Opinion in Neurobiology

Volume 67, April 2021, Pages 115-122
Current Opinion in Neurobiology

The homeostatic homunculus: rethinking deprivation-triggered reorganisation

https://doi.org/10.1016/j.conb.2020.08.008Get rights and content

Highlights

  • Homeostatic mechanisms may sustain persistent representation of a missing hand.

  • Recent evidence indicates distributed latent activity across the homunculus.

  • Deprivation uncovers pre-existing latent activity, that can manifest as remapping.

  • Remapping could in some instances correspond to stabilising homeostatic mechanisms.

While amputation was considered a prominent model for cortical reorganisation, recent evidence highlights persistent representation of the missing hand. We offer a new perspective on the literature of amputation-triggered sensorimotor plasticity, by emphasising the need for homeostasis and emerging evidence of latent activity distributed across the homunculus. We argue that deprivation uncovers pre-existing latent activity, which can manifest as remapping, but that since this activity was already there, remapping could in some instances correspond to functional stability of the system rather than reorganisation. Adaptive behaviour and Hebbian-like plasticity may also play crucial roles in maintaining the functional organisation of the homunculus when deprivation occurs in adulthood or in early development. Collectively, we suggest that the brain’s need for stability may underlie several key phenotypes for brain remapping, previously interpreted as consequential to reorganisation. Nevertheless, reorganisation may still be possible, especially when cortical changes contribute to the stability of the system.

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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