Summary Tinnitus is a common disorder characterized by ringing in the ear in the absence of sound. Converging evidence suggests that tinnitus pathophysiology involves damage to peripheral and/or central auditory pathways. However, whether auditory system dysfunction is sufficient to explain chronic tinnitus is unclear, especially in light of evidence implicating other networks, including the limbic system. Using functional magnetic resonance imaging and voxel-based morphometry, we assessed tinnitus-related functional and anatomical anomalies in auditory and limbic networks. Moderate hyperactivity was present in the primary and posterior auditory cortices of tinnitus patients. However, the nucleus accumbens exhibited the greatest degree of hyperactivity, specifically to sounds frequency-matched to patients’ tinnitus. Complementary structural differences were identified in ventromedial prefrontal cortex, another limbic structure heavily connected to the nucleus accumbens. Furthermore, tinnitus-related anomalies were intercorrelated in the two limbic regions and between limbic and primary auditory areas, indicating the importance of auditory-limbic interactions in tinnitus.

Debates about motor theories of speech perception have recently been reignited by a burst of reports implicating premotor cortex (PMC) in speech perception. Often, however, these debates conflate perceptual and decision processes. Evidence that PMC activity correlates with task difficulty and subject performance suggests that PMC might be recruited, in certain cases, to facilitate category judgments about speech sounds (rather than speech perception, which involves decoding of sounds). However, it remains unclear whether PMC does, indeed, exhibit neural selectivity that is relevant for speech decisions. Further, it is unknown whether PMC activity in such cases reflects input via the dorsal or ventral auditory pathway, and whether PMC processing of speech is automatic or task-dependent. In a novel modified categorization paradigm, we presented human subjects with paired speech sounds from a phonetic continuum but diverted their attention from phoneme category using a challenging dichotic listening task. Using fMRI rapid adaptation to probe neural selectivity, we observed acoustic-phonetic selectivity in left anterior and left posterior auditory cortical regions. Conversely, we observed phoneme-category selectivity in left PMC that correlated with explicit phoneme-categorization performance measured after scanning, suggesting that PMC recruitment can account for performance on phoneme-categorization tasks. Structural equation modeling revealed connectivity from posterior, but not anterior, auditory cortex to PMC, suggesting a dorsal route for auditory input to PMC. Our results provide evidence for an account of speech processing in which the dorsal stream mediates automatic sensorimotor integration of speech and may be recruited to support speech decision tasks.

Converging evidence supports the hypothesis that an antero-lateral processing pathway mediates sound identification in auditory cortex, analogous to the role of the ventral cortical pathway in visual object recognition. Studies in nonhuman primates have characterized the antero-lateral auditory pathway as a processing hierarchy, composed of three anatomically and physiologically distinct initial stages: core, belt and parabelt. In humans, potential homologues of these regions have been identified anatomically, but reliable and complete functional distinctions between them have yet to be established. Because the anatomical locations of these fields vary across subjects, investigations of potential homologues between monkeys and humans require these fields to be defined in single subjects. Using functional MRI, we presented three classes of sounds (tones, band-passed noise bursts, and conspecific vocalizations), equivalent to those used in previous monkey studies. In each individual subject, three regions showing functional similarities to macaque core, belt and parabelt were readily identified. Furthermore, the relative sizes and locations of these regions were consistent with those reported in human anatomical studies. Our results demonstrate that the functional organization of the antero-lateral processing pathway in humans is largely consistent with that of nonhuman primates. Because our scanning sessions last only 15 min/subject, they can be run in conjunction with other scans. This will enable future studies to characterize functional modules in human auditory cortex at a level of detail previously possible only in visual cortex. Furthermore, the approach of employing identical schemes in both humans and monkeys will aid with establishing potential homologies between them.