Adaptive, behaviorally gated, persistent encoding of task-relevant auditory information in ferret frontal cortex

Abstract

Top-down signals from frontal cortex (FC) are conjectured to play a critical role in cognitive control of sensory processing. To explore this interaction, we compared activity in ferret FC and primary auditory cortex (A1) during auditory and visual tasks requiring discrimination between classes of reference and target stimuli. FC responses were behaviorally-gated, selectively encoded the timing and invariant behavioral meaning of target stimuli, could be rapid in onset, and sometimes persisted for hours following behavior. This mirrors earlier findings in A1that attention triggered rapid, selective, persistent, task-related changes in spectrotemporal receptive fields. Simultaneously recorded local field potentials (LFPs) revealed behaviorally-gated changes in inter-areal coherence, selectively modulated between FC and focal regions of A1 responsive to target sounds. These results suggest that A1 and FC dynamically establish a functional connection during auditory behavior that shapes the flow of sensory information and maintains a persistent trace of recent task-relevant stimulus features.

Rapid Spectrotemporal Plasticity in Primary Auditory Cortex during Behavior

“…The task design and behavioral training procedure were the same as in our previous study (for further details, see Yin et al, 2010). In brief, each trial was initiated when the animal refrained from licking the waterspout for a minimum of 0.5 s. In each trial, a random number (1-5) of reference tone sequences (nontarget) sharing the same frequency contour (either Step-Up or Step-Down for a given animal) was presented, followed by a target tone sequence with the opposite frequency contour.…”

“…Instead, ferrets had to integrate the first tone (T1) with the second tone (T2) together and use the relationship between the two tones to determine pitch direction. Eventually, after several months of shaped training (Yin et al, 2010), the animals learned to attend to relative pitch change regard- Figure 1. Structure of the behavioral tasks in two animals.…”

“…The bar plot represented the average DI when the animal performed the task with its head restrained. The dashed horizontal lines indicate the threshold level defined as the mean ϩ 2 SD of the shuffled DIs (for more details, see Yin et al, 2010). There was no difference in performance between the experimental conditions with and without the TORCs.…”

“…This task-related optimization is influenced by context and task properties (task design, reward valence), by animal training history and motivation, and by the specific sensory stimuli involved (Beitel et al, 2003;Fritz et al, , 2005aFritz et al, , b, 2007Fritz et al, , 2010Brown et al, 2004;Blake et al, 2006;Polley et al, 2006;Selezneva et al, 2006;David et al, 2012;Guo et al, 2013). Thus, when detecting a target tone against a noisy background, the sensitivity of the receptive fields in primary auditory cortex (A1) rapidly changes at the frequency of the target tone Atiani et al, 2009).…”

“…This study tested the postulate that complex spectrotemporal stimuli would induce a matching spectrotemporal pattern of rapid plasticity. We tested this hypothesis in ferrets trained to discriminate the direction of a variable frequency two-tone pair (Yin et al, 2010). These ferrets learned to distinguish the direction of a twotone contour independent of the absolute frequency of the tone components.…”