Testing the perilesional neuroplastic recruitment hypothesis in aphasia

Abstract Objective A prominent theory proposes that neuroplastic recruitment of perilesional tissue supports aphasia recovery, especially when language-capable cortex is spared by smaller lesions. This theory has rarely been tested directly, and findings have been inconclusive. Here, we test the perilesional plasticity hypothesis using two fMRI tasks in two groups of stroke survivors. Methods Two cohorts totaling 84 chronic left-hemisphere stroke survivors with prior aphasia diagnosis, and 80 control participants underwent fMRI using either a naming task or a reliable semantic decision task. Individualized perilesional tissue was defined by dilating anatomical lesions, and language regions were defined using meta-analyses. Mixed modeling examined differences in activity between groups. Relationships with lesion size and aphasia severity were examined. Results Stroke survivors exhibited reduced activity in perilesional language tissue relative to controls in both tasks. Although a few cortical regions exhibited greater activity irrespective of distance from the lesion, or only when distant from the lesion, no regions exhibited increased activity only when near the lesion. Larger lesions were associated with reduced language activity irrespective of distance from the lesion. Using the reliable fMRI task, reduced language activity related to aphasia severity independent of lesion size. Interpretation We find no evidence for neuroplastic recruitment of perilesional tissue in aphasia beyond its typical role in language. Rather, our findings are consistent with alternative hypotheses that left-hemisphere activation changes during recovery relate to normalization of language network dysfunction and possibly recruitment of alternate cortical processors. These findings clarify left-hemisphere neuroplastic mechanisms supporting language recovery after stroke. Summary for Social Media If Accepted Twitter handle @crlgeorgetown What is the current knowledge on the topic? After left-hemisphere stroke, many individuals experience long-term language impairment (aphasia) while others recover their communication abilities. Although there are several hypotheses concerning the kind of brain neuroplasticity that allows some individuals to recover, these mechanisms are not understood in aphasia. What question did this study address? This study tested the perilesional plasticity hypothesis as it relates to aphasia recovery. This predominant theory posits that tissue around the stroke lesion boundary becomes recruited to support recovered language function in post-stroke aphasia. What does this study add to our knowledge? This study clarifies the mechanisms of neuroplasticity in stroke aphasia recovery. The results are not consistent with the conventional perilesional plasticity hypothesis, but rather favor an interpretation that recovery is supported by normalization of language network dysfunction and possibly recruitment of alternate brain regions How might this potentially impact on the practice of neurology? These conclusions will give practicing neurologists a better understanding of how the brain recovers from aphasia after stroke.