Modular reconfiguration of an auditory-control brain network supports adaptive listening behavior

Abstract

AbstractSpeech comprehension in noisy, multi-talker situations poses a challenge. Human listeners differ substantially in the degree to which they adapt behaviorally and can listen successfully under such circumstances. How cortical networks embody this adaptation, particularly at the individual level, is currently unknown. We here explain this adaptation from reconfiguration of brain networks for a challenging listening task (i.e., a novel linguistic variant of the Posner paradigm with concurrent speech) in an age-varying sample of N = 49 healthy adults undergoing resting-state and task fMRI. We here provide evidence for the hypothesis that more successful listeners exhibit stronger task-specific reconfiguration, hence better adaptation, of brain networks. From rest to task, brain networks become reconfigured towards more localized cortical processing characterized by higher topological segregation. This reconfiguration is dominated by the functional division of an auditory and a cingulo-opercular module, and the emergence of a conjoined auditory and ventral attention module along bilateral middle and posterior temporal cortices. Supporting our hypothesis, the degree to which modularity of this fronto-temporal auditory-control network is increased relative to resting state predicts individuals’ listening success in states of divided and selective attention. Our findings elucidate how fine-tuned cortical communication dynamics shape selection and comprehension of speech. Our results highlight modularity of the auditory-control network as a key organizational principle in cortical implementation of auditory spatial attention in challenging listening situations.Significance StatementHow do brain networks shape our listening behavior? We here develop and test the hypothesis that, during challenging listening situations, intrinsic brain networks are reconfigured to adapt to the listening demands, and thus to enable successful listening. We find that, relative to a task-free resting state, networks of the listening brain show higher segregation of temporal auditory, ventral attention, and frontal control regions known to be involved in speech processing, sound localization, and effortful listening. Importantly, the relative change in modularity of this auditory-control network predicts individuals’ listening success. Our findings shed light on how cortical communication dynamics tune selection and comprehension of speech in challenging listening situations, and suggest modularity as the network principle of auditory spatial attention.