Temporo-cerebellar connectivity underlies timing constraints in audition

Abstract

The flexible and efficient adaptation to dynamic, rapid changes in the auditory environment likely involves generating and updating of internal models. Such models arguably exploit connections between the neocortex and the cerebellum, supporting proactive adaptation. Here we test the functional mechanisms associated with temporo-cerebellar connectivity, verifying these mechanisms for speech sounds. First, we identify lesion-specific deficits for the encoding of short timescale spectro-temporal non-speech and speech properties in patients with left posterior temporal cortex stroke. Second, using lesion-guided probabilistic tractography in healthy participants, we reveal bidirectional temporo-cerebellar connectivity with cerebellar dentate nuclei and crura I/II. These findings imply that the encoding and modeling of rapidly modulated auditory spectro-temporal properties engage a temporo-cerebellar interface. The data further support the conjecture that proactive adaptation to a dynamic environment via internal models is a generalizable principle. Significance StatementAsymmetric sampling in time, the principle of duration-sensitive hemispheric specialization of the cerebral cortex in the sensory decomposition of sound, is a widely tested hypothesis in auditory neuroscience. This functional organization is mirrored in the cerebellar cortex, implicated in the internal forward-modeling of sensory feedback that arises from motor actions. The potential structural and functional integration of these systems is not well understood. Using a unique combination of causal lesion-symptom mapping in persons with temporal lobe damage and diffusion-weighted magnetic resonance neuroimaging in healthy persons, we identify one key missing link and provide evidence for cross-lateral temporo-cerebellar connectivity using probabilistic white matter fiber tractography. These cerebellar-pontine-temporal cortex connections not only support asymmetric sampling in time but also establish the basis for a generalizable role of cerebellar forward-modeling in sensation beyond the monitoring of sensory feedback in the motor domain.