Auditory Cortical Gradients Integrate Bottom-Up and Top-Down Structure During Natural Sound Categorisation

Abstract

Understanding how the brain organises natural categories is a central challenge in neuroscience. While prior work has shown that categories can be decoded from distributed activity patterns in auditory cortex, it remains unclear how these categories are globally arranged relative to one another, and how low-level acoustic and higher-level semantic structure jointly shape this organisation. Here, we addressed these questions by deriving low-dimensional functional gradients from high-depth functional magnetic resonance imaging (fMRI) data (three participants, [~]4.7 hours each) acquired during a category-specific one-back task. These gradients captured the principal axes of population activity in auditory cortex. Gradient-based models of the auditory cortex explained category structure more accurately than region-of-interest or whole-brain approaches, revealing that category information is distributed across multiple continuous axes rather than aligned with any single organisational dimension. Projecting acoustic (gammatone filter-bank) and behavioural similarity spaces directly into a shared framework with the fMRI functional axes showed that both contribute to the brains category geometry, with acoustic structure exerting a somewhat stronger influence. However, representational relationships varied across category pairs: some reflected primarily acoustic similarity, others semantic distinctions, and many a combination of both. This pairwise heterogeneity shows how auditory cortex may integrate multiple representational dimensions that define higher-level categories. Significance StatementCategorising natural sounds requires the brain to transform diverse acoustic signals into meaningful concepts. How this is achieved remains unclear: prior work has shown distributed activation patterns in auditory cortex, but not how category relationships are organised within its functional architecture. We show that natural sound categories are embedded across continuous cortical gradients that integrate bottom-up acoustic structure with top-down semantic information. Different categories emerge as flexible combinations of these spectral and behavioural dimensions. These findings reveal that natural sound categorisation arises from the geometry of cortical organisation, moving beyond localist accounts and offering a new framework for understanding how perception and cognition are linked in the human auditory system.