Abstract
Primary sensory cortices are classically considered to extract and represent stimulus features, while association and higher-order areas are thought to carry information about stimulus meaning. Here we show that this information can in fact be found in the neuronal population code of the primary auditory cortex (A1). A1 activity was recorded in awake ferrets while they either passively listened or actively discriminated stimuli in a range of Go/No-Go paradigms, with different sounds and reinforcements. Population-level dimensionality reduction techniques reveal that task engagement induces a shift in stimulus encoding from a sensory to a behaviorally driven representation that specifically enhances the target stimulus in all paradigms. This shift partly relies on task-engagement-induced changes in spontaneous activity. Altogether, we show that A1 population activity bears strong similarities to frontal cortex responses. These findings indicate that primary sensory cortices implement a crucial change in the structure of population activity to extract task-relevant information during behavior.
Highlights
Primary sensory cortices are classically considered to extract and represent stimulus features, while association and higher-order areas are thought to carry information about stimulus meaning
Effects of task engagement have been investigated in the auditory cortex, where it was found that receptive fields of primary auditory cortex neurons adapt rapidly to behavioral demands when animals engage in various types of auditory discrimination tasks[26,27,28,29,30]
We show that simple population analyses reveal that task engagement induces a shift in the primary auditory cortex from a sensory-driven representation to a representation of the behavioral meaning of stimuli, analogous to the one found in the frontal cortex
Summary
Primary sensory cortices are classically considered to extract and represent stimulus features, while association and higher-order areas are thought to carry information about stimulus meaning. They integrate inputs from different sensory modalities, transform sensory information into categorical percepts and decisions, and store them in working memory until the time when the appropriate motor action needs to be executed[5,6] According to this classical feedforward picture, primary sensory areas are often considered as playing a largely static role in extracting and encoding high-level stimulus physical attributes[7,8,9,10]. Effects of task engagement have been investigated in the auditory cortex, where it was found that receptive fields of primary auditory cortex neurons adapt rapidly to behavioral demands when animals engage in various types of auditory discrimination tasks[26,27,28,29,30] These observations have been interpreted as signatures of highly flexible sensory representations in primary cortical areas, and they raise the possibility that these areas may be performing computations more complex than simple extraction and transmission of stimulus features to higher-order regions. This shift was in part enabled by a novel mechanism based on the change in the pattern of spontaneous activity during task engagement
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