Task Engagement Enhances Population Encoding of Stimulus Meaning in Primary Auditory Cortex

Abstract

The main functions of primary sensory cortical areas are classically considered to be the extraction and representation of stimulus features. In contrast, higher cortical sensory association areas are thought to be responsible for combining these sensory representations with internal motivations and learnt associations. These regions generate appropriate neural responses that are maintained until a motor command is executed. Within this framework, responses of the primary sensory areas during task performance are expected to carry less information about the behavioral meaning of the stimulus than higher sensory, association, motor and frontal cortices. Here we demonstrate instead that the neuronal population responses in the early primary auditory cortex (A1) display many aspects of responses generally associated with higher-level areas. A1 activity was recorded in awake ferrets while they were either passively listening or actively discriminating two periodic click trains of different rates in a Go/No-Go paradigm. By applying population-level dimensionality reduction techniques, we found that task-engagement induced a shift in the nature of the encoding from a sensory-driven representation of the two stimuli to a behaviorally relevant representation of the two categories that specifically enhances the target stimulus. We demonstrate that this shift in encoding relies partly on a novel mechanism of change in spontaneous activity patterns upon engagement in the task. We show that this population-level representation of stimuli in A1 population activity bears strong similarities to responses in the frontal cortex, but appears earlier following stimulus presentation. Analysis of neural activity recorded in various Go/No-Go tasks, with different sounds and reinforcement paradigms, reveals that this striking population-level enhancement of target representation is a general property of task engagement. These findings indicate that primary sensory cortices play a highly flexible role in the processing of incoming stimuli and implement a crucial change in the structure of population activity in order to extract task-relevant information during behavior.

Using Temporal Expectation to Assess Auditory Streaming in Mice

“…This was surprising, as the activity in auditory cortex is traditionally thought of as dedicated to the processing of auditory signals. These modulations might instead reflect the encoding of other task aspects, such as movement preparation, reward expectation, or task rule (Hu, 2003 ; Shuler and Bear, 2006 ; Rodgers and DeWeese, 2014 ; Bagur et al, 2017 ). Neural activity at the level of AC has recently been proposed to encode more than simply stimulus features (Rodgers and DeWeese, 2014 ; Bagur et al, 2017 ; Francis et al, 2018 ), however the underlying mechanisms are yet unknown.…”

“…These modulations might instead reflect the encoding of other task aspects, such as movement preparation, reward expectation, or task rule (Hu, 2003 ; Shuler and Bear, 2006 ; Rodgers and DeWeese, 2014 ; Bagur et al, 2017 ). Neural activity at the level of AC has recently been proposed to encode more than simply stimulus features (Rodgers and DeWeese, 2014 ; Bagur et al, 2017 ; Francis et al, 2018 ), however the underlying mechanisms are yet unknown. Future experiments will enable to delineate the contribution of specific anatomical pathways, including both sub-cortical (Thorn et al, 2010 ; Froemke et al, 2012 ; Pinto et al, 2013 ; Wimmer et al, 2015 ; Nelson and Mooney, 2016 ) and cortical structures (Gremel and Costa, 2013 ; Rodgers and DeWeese, 2014 ; Winkowski et al, 2017 ), in the modulation of AC activity during varying attentional states.…”

From Stimulus to Behavioral Decision-Making

“…This was surprising, as the activity in auditory cortex is traditionally thought of as dedicated to the processing of auditory signals. These modulations might instead reflect the encoding of other task aspects, such as movement preparation, reward expectation, or task rule (Hu, 2003;Shuler and Bear, 2006;Rodgers and DeWeese, 2014;Bagur et al, 2017). Neural activity at the level of AC has recently been proposed to encode more than simply stimulus features (Rodgers and DeWeese, 2014;Bagur et al, 2017;Francis et al, 2018), however the underlying mechanisms are yet unknown.…”

Implantable Neural Interfaces and Wearable Tactile Systems for Bidirectional Neuroprosthetics Systems

“…Comparison among different strategies of stimulation of PNS to evoke tactile percepts. Parameters that have been considered are: i) number of subjects (S) and implant duration; ii) type of implanted electrode, number of channels, nerve target; iii) impedance measurement; iv) type of stimulation pattern; v) threshold charge/current over time; vi) …”

“…Plexon offers solutions data acquisition and stimulation systems but also electrodes for research needs for cortical recordings (channel counts up to 32 with platinum–iridium contacts) …”