Associations between sounds and actions in early auditory cortex of nonhuman primates

Abstract

An individual may need to take different actions to the same stimulus in different situations to achieve a given goal. The selection of the appropriate action hinges on the previously learned associations between stimuli, actions, and outcomes in the situations. Here, using a go/no-go paradigm and a symmetrical reward, we show that early auditory cortex of nonhuman primates represents such associations, in both the spiking activity and the local field potentials. Sound-evoked neuronal responses changed with sensorimotor associations shortly after sound onset, and the neuronal responses were largest when the sound signaled that a no-go response was required in a trial to obtain a reward. Our findings suggest that association processes take place in the auditory system and do not necessarily rely on association cortex. Thus, auditory cortex may contribute to a rapid selection of the appropriate motor responses to sounds during goal-directed behavior.

Task rule and choice are reflected by layer-specific processing in rodent auditory cortical microcircuits

“…This is in accordance with the findings that neurons in these layers convey information to downstream motor centers, as the basal ganglia or the striatum, which play an important role for the control of motor decisions by the sensory cortex (Xiong et al, 2015;Znamenskiy and Zador, 2013). Further, the selection of an appropriate action might also be conveyed directly to motor cortex via direct anatomical projections (Matyas et al, 2010;Huang et al, 2019). Ample evidence argues that our findings reflect a motor-related modulation of the cortical physiology, rather than a movement artifact.…”

“…Motor initiation has been reported before to enhance or suppress sensory-driven activity in other (primary) sensory cortices depending on region, system and taskengagement (Busse et al, 2017;Steinmetz et al, 2019). From our data we hypothesize, that, during the detection, the tone-evoked activity in the primary auditory cortex may be modulated by auditory-guided motor initiation (Brosch et al, 2015;Huang et al, 2019;Niwa et al, 2012a). The distinct sound frequency of a pure tone seems less determining on the activity strength.…”

“…While several studies also observed an enhanced representation of target stimuli that initiated an auditoryguided motor response in various Go/NoGo discrimination tasks (Bagur et al, 2018;Fritz et al, 2003;Gold et al, 1999), others found higher cortical recruitment during correct rejections compared to hit trials in a Go/NoGo task in the macaque A1 (Huang et al, 2019). Previous findings demonstrate the potentially inherent neuronal variability comprised of the exact task design at hand, aversive or appetitive reinforcing regimes, and stimulus characteristics which may partially explain contradictory findings (David et al, 2012;Osmanski and Wang, 2015) and needs further evaluation.…”

“…In the case of the auditory system, ample evidence has revealed that the primary auditory cortex (A1) integrates sensory information with other contextual and motor signals and further reflects higher cognitive demands responsible for prediction (Kumar et al, 2011;Parras et al, 2017;Town et al, 2018), choice accuracy (Niwa et al, 2012;Caras & Sanes, 2017), and auditory-guided decision making (Brosch et al, 2005;King et al, 2018;Ohl and Scheich, 2005;Tsunada et al, 2015). The salience of behaviorally relevant sounds further critically depends on the exact reinforcement regimes and task rules (Bagur et al, 2018;David et al, 2012;Huang et al, 2019), which renders the auditory cortex a multifarious integrative circuit. These and other studies have described corresponding neural correlates on the level of single neuron or population activity recordings.…”

Correlates of auditory decision making in prefrontal, auditory, and basal lateral amygdala cortical areas

“…Previous work has shown that AC neurons can encode non-sensory, choice-related activity (Huang, Heil et al 2019). The Huang et al study found that whether a response was predictable following a cue tone, based on the task condition, affected neural responses in AC to the tone.…”