Auditory corticostriatal connections in the human brain

Abstract

Auditory learning depends on sensory, perceptual, decisional, and reward-based processes that are supported by the dorsal striatum. Auditory corticostriatal connections have been well-characterized in animal models including non-human primates, where primary auditory cortex preferentially connects to putamen, and caudate head receives most of its inputs from anterior superior temporal cortex. However, the extent to which human auditory corticostriatal connectivity follows similar organizational principles is challenging to assess due to the density of these striatal structures relative to the resolution of traditional diffusion MRI techniques, as well as dorsal striatums location near multiple major crossing white matter bundles. We leveraged high-quality diffusion-weighted MRI tractography to virtually dissect structural pathways between auditory cortical regions and dorsal striatal regions in a sub-millimeter resolution single-participant dataset. Across most of auditory cortex, putamen connections were more frequent than caudate connections; only anterior-most superior temporal cortex had strong connectivity with caudate, specifically the caudate head. Putamen streamline endpoints were largely along the ventral portion of the structure, ranging from caudal to middle putamen. These results were consistent across analysis and tractography pipelines. In contrast to the auditory findings, visual corticostriatal streamlines did not preferentially reach putamen. We replicate these results in an independent sample of near-millimeter resolution single-session diffusion MRI from the Human Connectome Project. Overall, our results suggest strong structural connectivity between primary and association auditory cortices with putamen but not with any subdivision of caudate. Prioritized connectivity between superior temporal cortex and putamen is highly suggestive of distinct functional roles for striatal subdivisions in auditory perception.