Central activation deficits contribute to post stroke lingual weakness in a rat model.

Abstract

Lingual weakness frequently occurs after stroke and is associated with deficits in speaking and swallowing. Chronic weakness after stroke has been attributed to both impaired central activation of target muscles and reduced force-generating capacity within muscles. How these factors contribute to lingual weakness is not known. We hypothesized that lingual weakness due to middle cerebral artery occlusion (MCAO) would manifest as reduced muscle force capacity and reduced muscle activation. Rats were randomized into MCAO or sham surgery groups. Maximum volitional tongue forces were quantified 8 wk after surgery. Hypoglossal nerve stimulation was used to assess maximum stimulated force, muscle twitch properties, and force-frequency response. The central activation ratio was determined by maximum volitional/maximum stimulated force. Genioglossus muscle fiber type properties and neuromuscular junction innervation were assessed. Maximum volitional force and the central activation ratio were significantly reduced with MCAO. Maximum stimulated force was not significantly different. No significant differences were found for muscle twitch properties, unilateral contractile properties, muscle fiber type percentages, or fiber size. However, the twitch/tetanus ratio was significantly increased in the MCAO group relative to sham. A small but significant increase in denervated neuromuscular junctions (NMJs) and fiber-type grouping occurred in the contralesional genioglossus. Results suggest that the primary cause of chronic lingual weakness after stroke is impaired muscle activation rather than a deficit of force-generating capacity in lingual muscles. Increased fiber type grouping and denervated NMJs in the contralesional genioglossus suggest that partial reinnervation of muscle fibers may have preserved force-generating capacity, but not optimal activation patterns.NEW & NOTEWORTHY Despite significant reductions in maximum volitional forces, the intrinsic force-generating capacity of the protrusive lingual muscles was not reduced with unilateral cerebral ischemia. Small yet significant increases in denervated NMJs and fiber-type grouping of the contralesional genioglossus suggest that the muscle underwent denervation and reinnervation. Together these results suggest that spontaneous neuromuscular plasticity was sufficient to prevent atrophy, yet central activation deficits remain and contribute to chronic lingual weakness after stroke.