A neuroanatomical framework for upper limb synergies after stroke

Abstract

Muscle synergies describe common patterns of co- or reciprocal activation that occur during movement. After stroke, these synergies change, often in stereotypical ways. The mechanism underlying this change reflects damage to key motor pathways as a result of the stroke lesion, and the subsequent reorganization along the neuroaxis, which may be further detrimental or restorative to motor function. The time course of abnormal synergy formation seems to lag spontaneous recovery that occurs in the initial weeks after stroke. In healthy individuals, motor cortical activity, descending via the corticospinal tract (CST) is the predominant driver of voluntary behavior. When the CST is damaged after stroke, other descending pathways may be up-regulated to compensate. The contribution of these pathways may emerge as new synergies take shape at the chronic stage after stroke, as a result of plasticity along the neuroaxis. The location of the stroke lesion and properties of the secondary descending pathways and their regulation are then critical for shaping the synergies in the remaining motor behavior. A consideration of the integrity of remaining descending motor pathways may aid in the design of new rehabilitation therapies.

Keywords: corticospinal tract; muscle synergy; proximal–distal patterning; stroke; upper limb.

Figures

Figure 1

A schematic of descending pathways involved in the formation of synergies in healthy motor behavior, and their disruption after stroke. Direct CST connections exist from the cortex to motor neuron pools predominantly for distal muscles, green pathways from C1 to C5. Other CST connections, dark gray pathways from C2 and C3, carry low-dimensional motor commands and innervate synergy-forming spinal modules S1 and S2, which in turn have divergent connections to multiple motor neuron pools at several rostrocaudal levels. Red lines from C4 represent a cortically derived synergy controlling the three proximal motor neuron pools. Connections from C4 and C5 normally inhibit the contralateral motor cortex. Among other functions, this transcallosal input regulates alternate descending pathways like the CRPP (blue lines), which innervates propriospinal neurons linking multiple proximal limb segments. Dark red and wavy horizontal lines indicate sites of damage caused by three stroke lesions. Lesion 1 disrupts low-dimensional information from C3 to the synergy module at S1, and therefore would interfere with activation of the whole synergy mediated by S1, while leaving the synergy structure intact. Lesion 2 represents a mild event, transecting part of the cortically derived synergy from C4, which would alter its structure. Lesion 2 also damages transcallosal connections to the contralesional hemisphere, reducing interhemispheric inhibition and up-regulating the CRPP and other alternate, ipsilateral descending pathways. Since the lesion only affects a small number of CST fibers, remaining descending connections will subsume the damaged functions, and prognosis is good. The up-regulated CRPP interferes with productive CST drive. Suppression of the contralesional hemisphere by non-invasive brain stimulation, for example, c-tDCS, may reduce CRPP activity and thus be beneficial. Lesion 3 is larger than lesion 2, resulting in a severe impairment. Here, the CRPP represents the majority of remaining drive, meaning that c-tDCS of the contralesional hemisphere could be disadvantageous [c.f., Bradnam et al. (2012)].