A Cortico-Collicular Amplification Mechanism for Gap Detection

• Published in: Cerebral cortex (New York, N.Y. 1991) N.Y. 1991), 2020-05, Vol.30 (6), p.3590-3607
• Main Authors: Weible, Aldis P, Yavorska, Iryna, Wehr, Michael
• Format: Article
• Language: English
• Subjects: Acoustic Stimulation; Animals; Auditory Cortex - cytology; Auditory Cortex - physiology; Auditory Pathways - physiology; Auditory Perception - physiology; Inferior Colliculi - cytology; Inferior Colliculi - physiology; Mice; Neural Pathways; Neurons - physiology; Optogenetics; Original; Signal Detection, Psychological; Time Perception - physiology
• ISSN: 1047-3211; 1460-2199
• DOI: 10.1093/cercor/bhz328

Abstract Auditory cortex (AC) is necessary for the detection of brief gaps in ongoing sounds, but not for the detection of longer gaps or other stimuli such as tones or noise. It remains unclear why this is so, and what is special about brief gaps in particular. Here, we used both optogenetic suppression and conventional lesions to show that the cortical dependence of brief gap detection hinges specifically on gap termination. We then identified a cortico-collicular gap detection circuit that amplifies cortical gap termination responses before projecting to inferior colliculus (IC) to impact behavior. We found that gaps evoked off-responses and on-responses in cortical neurons, which temporally overlapped for brief gaps, but not long gaps. This overlap specifically enhanced cortical responses to brief gaps, whereas IC neurons preferred longer gaps. Optogenetic suppression of AC reduced collicular responses specifically to brief gaps, indicating that under normal conditions, the enhanced cortical representation of brief gaps amplifies collicular gap responses. Together these mechanisms explain how and why AC contributes to the behavioral detection of brief gaps, which are critical cues for speech perception, perceptual grouping, and auditory scene analysis.