Hierarchical differences in the encoding of sound and choice in the subcortical auditory system

J Neurophysiol. 2023 Mar 1;129(3):591-608. doi: 10.1152/jn.00439.2022. Epub 2023 Jan 18.

Abstract

Detection of sounds is a fundamental function of the auditory system. Although studies of auditory cortex have gained substantial insight into detection performance using behaving animals, previous subcortical studies have mostly taken place under anesthesia, in passively listening animals, or have not measured performance at threshold. These limitations preclude direct comparisons between neuronal responses and behavior. To address this, we simultaneously measured auditory detection performance and single-unit activity in the inferior colliculus (IC) and cochlear nucleus (CN) in macaques. The spontaneous activity and response variability of CN neurons were higher than those observed for IC neurons. Signal detection theoretic methods revealed that the magnitude of responses of IC neurons provided more reliable estimates of psychometric threshold and slope compared with the responses of single CN neurons. However, pooling small populations of CN neurons provided reliable estimates of psychometric threshold and slope, suggesting sufficient information in CN population activity. Trial-by-trial correlations between spike count and behavioral response emerged 50-75 ms after sound onset for most IC neurons, but for few neurons in the CN. These results highlight hierarchical differences between neurometric-psychometric correlations in CN and IC and have important implications for how subcortical information could be decoded.NEW & NOTEWORTHY The cerebral cortex is widely recognized to play a role in sensory processing and decision-making. Accounts of the neural basis of auditory perception and its dysfunction are based on this idea. However, significantly less attention has been paid to midbrain and brainstem structures in this regard. Here, we find that subcortical auditory neurons represent stimulus information sufficient for detection and predict behavioral choice on a trial-by-trial basis.

Keywords: cochlear nucleus; detection; inferior colliculus; macaque.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Acoustic Stimulation
  • Animals
  • Auditory Cortex* / physiology
  • Auditory Pathways / physiology
  • Auditory Perception / physiology
  • Cochlear Nucleus* / physiology
  • Inferior Colliculi* / physiology
  • Neurons / physiology