A hierarchy of corticospinal plasticity in human hand and forearm muscles

Abstract

Key points Pairing stimulation of a finger flexor or extensor muscle at the motor point with transcranial magnetic stimulation (TMS) of the motor cortex generated plastic changes in motor output. Increases in output were greater in intrinsic hand muscles than in the finger flexor. No changes occurred in the finger extensor. This gradient was seen irrespective of which muscle was stimulated paired with transcranial magnetic stimulation. Intermittent theta‐burst stimulation also produced increases in output, although these were similar across muscles. We suggest that intrinsic hand and flexor muscles have a higher potential to show plasticity than extensors, although only when plasticity is induced by sensory input. This may relate to differences seen in recovery of function in these muscles after injury, such as post‐stroke. Abstract The ability of the motor system to show plastic change underlies skill learning and also permits recovery after injury. One puzzling observation is that, after stroke, upper limb flexor muscles show good recovery but extensors remain weak, with this being a major contributor to residual disability. We hypothesized that there might be differences in potential for plasticity across hand and forearm muscles. In the present study, we investigated this using two protocols based on transcranial magnetic brain stimulation (TMS) in healthy human subjects. Baseline TMS responses were recorded from two intrinsic hand muscles: flexor digitorum superficialis (FDS) and extensor digitorum communis (EDC). In the first study, paired associative stimulation (PAS) was delivered by pairing motor point stimulation of FDS or EDC with TMS. Responses were then remeasured. Increases were greatest in the hand muscles, smaller in FDS and non‐significant in EDC, irrespective of whether stimulation of FDS or EDC was used. In the second study, intermittent theta‐burst rapid rate TMS was applied instead of PAS. In this case, all muscles showed similar increases in TMS responses. We conclude that the potential to show plastic changes in motor cortical output has the gradient: hand muscles > flexors > extensors. However, this was only seen in a protocol that requires integration of sensory input (PAS) and not when plasticity was induced purely by cortical stimulation (rapid rate TMS). This observation may relate to why functional recovery tends to favour flexor and hand muscles over extensors.

Induction of plasticity in the human motor system by motor imagery and transcranial magnetic stimulation

“…These are promising results, but we recently showed that, in the upper limb, protocols which use sensory input to generate plasticity may have an intrinsic bias towards certain muscle groups. We showed that it was possible to generate robust changes generated in flexor and intrinsic hand muscles, but minimal effects in extensors (Foysal & Baker, 2019). Interestingly, this bias was not seen in a protocol which used only TMS, without paired sensory input.…”

Disparity among muscles: different levels of plasticity of cortical representation of different muscles revealed by transcranial magnetic stimulation

“…In dystonia, the abnormality of sensory-motor plasticity might represent an endophenotypic trait that predisposes to the development of dystonia while in stroke patients it might be the structural brain lesion that results in a hand posture abnormality by interacting with an innate physiological asymmetry in the level of plasticity of cortical areas controlling different muscles. Of note is that the PAS protocol used by Riashad Foysal & Baker (2019), in which the motor point is stimulated instead of the peripheral nerve, seems not to have the same spatial specificity of the standard PAS described by Stefan et al (2000) in that stimulation of the motor point of either flexor digitorum superficialis or extensor digitorum communis induced plastic changes in both forearm flexors, and intrinsic hand muscles. The study by Riashad Foysal & Baker (2019) confirms that non-invasive brain stimulation techniques can provide unique insights into the physiological basis of human brain plasticity.…”

“…Of note is that the PAS protocol used by Riashad Foysal & Baker (2019), in which the motor point is stimulated instead of the peripheral nerve, seems not to have the same spatial specificity of the standard PAS described by Stefan et al (2000) in that stimulation of the motor point of either flexor digitorum superficialis or extensor digitorum communis induced plastic changes in both forearm flexors, and intrinsic hand muscles. The study by Riashad Foysal & Baker (2019) confirms that non-invasive brain stimulation techniques can provide unique insights into the physiological basis of human brain plasticity. The assessment of sensory-motor plasticity in stroke might be useful for the early detection of changes that might interfere with functional recovery and also for the development and implementation of strategies aimed at Perspectives J Physiol 597.10 preventing the deleterious consequences of maladaptive plasticity.…”

“…In this issue of Journal of Physiology the same group of researchers use a novel approach to determine whether specific characteristic of the intrinsic plasticity of human cortical circuits controlling flexor muscles might contribute to their propensity to develop spasticity after stroke (Riashad Foysal & Baker, 2019). To this end, they studied different forms of brain plasticity in healthy subjects using transcranial magnetic stimulation (TMS) techniques.…”

“…Although iTBS and PAS induce similar after-effects on motor cortex excitability, their physiological bases are thought to have different mechanisms given that they are differentially affected in some pathological conditions (Dileone et al 2016). Riashad Foysal & Baker (2019) compare the effects of PAS produced either by pairing motor cortex TMS with motor point stimulation of flexor digitorum superficialis or extensor digitorum communis muscles with those of iTBS in the same muscles. They find that while iTBS has similar effects on flexor and extensor muscles, the effects of PAS are present in the hand muscles and in flexor digitorum superficialis but absent in extensor digitorum communis.…”