Abstract
Background.
Upper-limb impairment in patients with chronic
stroke appears to be partly attributable to an upregulated
reticulospinal tract (RST). Here, we assessed whether the impact of
corticospinal (CST) and RST connectivity on motor impairment and
skill-acquisition differs in sub-acute stroke, using transcranial magnetic stimulation (TMS)–based proxy measures.
Methods.
Thirty-eight stroke survivors were randomized to either reach training
3-6 weeks post-stroke (plus usual care) or usual care only. At 3, 6 and
12 weeks post-stroke, we measured ipsilesional and contralesional
cortical connectivity (surrogates for CST and RST connectivity,
respectively) to weak pre-activated triceps and deltoid muscles with
single pulse TMS, accuracy of planar reaching movements, muscle strength
(Motricity Index) and synergies (Fugl-Meyer upper-limb score).
Results.
Strength and presence of synergies were associated with ipsilesional
(CST) connectivity to the paretic upper-limb at 3 and 12 weeks. Training
led to planar reaching skill beyond that expected from spontaneous
recovery and occurred for both weak and strong ipsilesional tract
integrity. Reaching ability, presence of synergies, skill-acquisition
and strength were not affected by either the presence or absence of
contralesional (RST) connectivity.
Conclusion. The degree of
ipsilesional CST connectivity is the main determinant of proximal
dexterity, upper-limb strength and synergy expression in sub-acute
stroke. In contrast, there is no evidence for enhanced contralesional
RST connectivity contributing to any of these components of impairment.
In the sub-acute post-stroke period, the balance of activity between CST
and RST may matter more for the paretic phenotype than RST upregulation
per se.
Introduction
Motor impairment after stroke is closely associated with ipsilesional corticospinal tract (CST) damage.1-4
In addition, recent data suggest that arm flexor synergies, finger
enslaving on the paretic side and mirror movements on the non-paretic
hand after stroke are all attributable to an increased influence of the
reticulospinal tract (RST) after damage to the CST.5-11 Studies in primates have shown that 6 months after a lesion in the pyramidal tract,12 there is upregulation of the RST. In patients with chronic
stroke, the incidence of contralesional connectivity to the ipsilateral
paretic limb is increased, particularly in patients with moderate to
severe paresis,13,14 suggesting a similar upregulation of RST activity during recovery.15 An unanswered question is the impact of this RST upregulation after the initial plegic stage3; does it contribute to, or impede recovery, or is it an epiphenomenon of recovery, neither good nor bad.7
Furthermore, it is unclear whether unwanted muscle synergies result
from actual upregulation of pre-existing cortico-reticulospinal
descending pathways or can be attributed instead to a relative imbalance
between them (in the absence of upregulation) and the CST.6
Using
transcranial magnetic stimulation (TMS), we sought to determine the
degree of ipsilesional and contralesional cortical connectivity to
paretic arm muscles in a group of patients with moderate to severe
stroke in the early sub-acute period. TMS of the human motor cortex in
one hemisphere can evoke responses in ipsilateral muscles with
characteristics compatible with activation of oligosynaptic
cortico-bulbospinal pathways,16 most likely representing cortico-reticulo-spinal connection.13,14,17-19 This provides an indirect method of assessing the excitability of the RST in stroke survivors.11,20-22
We further investigated the effect of these two forms of connectivity
on strength, synergies, planar reaching accuracy and capacity for
skill-acquisition. We examined inputs to proximal muscles involved in
planar reaching movements since these are thought to receive greater
reticulospinal inputs than distal arm muscles.16,23
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