Correlates of Auditory Decision-Making in Prefrontal, Auditory, and Basal Lateral Amygdala Cortical Areas

J Neurosci. 2021 Feb 10;41(6):1301-1316. doi: 10.1523/JNEUROSCI.2217-20.2020. Epub 2020 Dec 10.

Abstract

Spatial selective listening and auditory choice underlie important processes including attending to a speaker at a cocktail party and knowing how (or whether) to respond. To examine task encoding and the relative timing of potential neural substrates underlying these behaviors, we developed a spatial selective detection paradigm for monkeys, and recorded activity in primary auditory cortex (AC), dorsolateral prefrontal cortex (dlPFC), and the basolateral amygdala (BLA). A comparison of neural responses among these three areas showed that, as expected, AC encoded the side of the cue and target characteristics before dlPFC and BLA. Interestingly, AC also encoded the choice of the monkey before dlPFC and around the time of BLA. Generally, BLA showed weak responses to all task features except the choice. Decoding analyses suggested that errors followed from a failure to encode the target stimulus in both AC and dlPFC, but again, these differences arose earlier in AC. The similarities between AC and dlPFC responses were abolished during passive sensory stimulation with identical trial conditions, suggesting that the robust sensory encoding in dlPFC is contextually gated. Thus, counter to a strictly PFC-driven decision process, in this spatial selective listening task AC neural activity represents the sensory and decision information before dlPFC. Unlike in the visual domain, in this auditory task, the BLA does not appear to be robustly involved in selective spatial processing.SIGNIFICANCE STATEMENT We examined neural correlates of an auditory spatial selective listening task by recording single-neuron activity in behaving monkeys from the amygdala, dorsolateral prefrontal cortex, and auditory cortex. We found that auditory cortex coded spatial cues and choice-related activity before dorsolateral prefrontal cortex or the amygdala. Auditory cortex also had robust delay period activity. Therefore, we found that auditory cortex could support the neural computations that underlie the behavioral processes in the task.

Keywords: amygdala; auditory; auditory cortex; decision-making; prefrontal cortex; selective listening.

Publication types

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

MeSH terms

  • Acoustic Stimulation / methods
  • Animals
  • Auditory Cortex / diagnostic imaging
  • Auditory Cortex / physiology*
  • Auditory Perception / physiology*
  • Basolateral Nuclear Complex / diagnostic imaging
  • Basolateral Nuclear Complex / physiology*
  • Decision Making / physiology*
  • Macaca mulatta
  • Male
  • Photic Stimulation / methods
  • Prefrontal Cortex / diagnostic imaging
  • Prefrontal Cortex / physiology
  • Psychomotor Performance / physiology*