Dynamics and Hierarchical Encoding of Non-compact Acoustic Categories in Auditory and Frontal Cortex

• Published in: Current biology Vol. 30; no. 9; pp. 1649 - 1663.e5
• Main Authors: Yin, Pingbo, Strait, Dana L., Radtke-Schuller, Susanne, Fritz, Jonathan B., Shamma, Shihab A.
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 04.05.2020
• Subjects: auditory categorization; auditory cortex; ferret; frontal cortex; long-term memory; top-down modulation; frontal cortex; auditory cortex; top-down modulation; ferret; long-term memory; auditory categorization
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2020.02.047

Categorical perception is a fundamental cognitive function enabling animals to flexibly assign sounds into behaviorally relevant categories. This study investigates the nature of acoustic category representations, their emergence in an ascending series of ferret auditory and frontal cortical fields, and the dynamics of this representation during passive listening to task-relevant stimuli and during active retrieval from memory while engaging in learned categorization tasks. Ferrets were trained on two auditory Go-NoGo categorization tasks to discriminate two non-compact sound categories (composed of tones or amplitude-modulated noise). Neuronal responses became progressively more categorical in higher cortical fields, especially during task performance. The dynamics of the categorical responses exhibited a cascading top-down modulation pattern that began earliest in the frontal cortex and subsequently flowed downstream to the secondary auditory cortex, followed by the primary auditory cortex. In a subpopulation of neurons, categorical responses persisted even during the passive listening condition, demonstrating memory for task categories and their enhanced categorical boundaries. •Enhanced categorical representations in higher auditory areas during behavior•Distinct sensory and categorical information flows during categorization tasks•Separate neuronal groups with intrinsic versus task-induced categorical responses•Similar dynamics in different categorization tasks with distinct acoustic features Yin et al. show neuronal responses become progressively more categorical in higher auditory and frontal cortical areas during passive listening in trained ferrets, and more so during engagement in categorization tasks. The dynamics of categorical responses exhibit a cascading top-down modulation pattern opposite to the rapid bottom-up sensory flow.