The frontal cortex (FC) has been implicated in many of the cognitive and executive control functions required for goal-directed behavior (Komura et al., 2001; Bruni et al., 2015; Duan et al., 2021; Friedman and Robbins, 2021), including decision-making (Coley et al., 2021; Liu et al., 2021), response inhibition (Schiller et al., 2014; Li et al., 2020), working memory (O’Reilly and Frank, 2006; Miller et al., 2018; Wilhelm et al., 2023), attentional control (Zikopoulos and Barbas, 2007; Gregorlou et al., 2014), and adaptive modulation of sensory filters (Banerjee et al., 2020). In the auditory system, cortical neurons can rapidly adapt their receptive field tuning and spectrotemporal selectivity reflecting changing stimulus context and task conditions (Fritz et al., 2003, 2005, 2007; David et al., 2012; Yin et al., 2014; Elgueda et al., 2019). This task-related receptive field plasticity may be shaped by changing functional connectivity between FC and auditory cortex (Fritz et al., 2010; Sheikhattar et al., 2018; Yin et al., 2020). This adaptive capacity is critical since context can transform the behavioral meaning of incoming stimuli and even cause the same sound to mean two opposite things in different circumstances.
In this study, we explored the role of the FC in this adaptive decision-making process by employing the same sounds to signify diametrically opposite meanings depending on task context and reward valence. In one behavioral paradigm, upon hearing a Target sound, animals initiated licking to obtain a water reward (positive reward; P-paradigm). In the other paradigm, animals learned to stop licking for water when presented with the same Target stimulus in order to avoid a mild shock (negative reward; N-paradigm). In an earlier study (David et al., 2012), we found that such different task reward structures and stimulus-action contingencies induced two strikingly distinct forms of receptive field plasticity in primary auditory cortex (A1). In light of the strong top-down projections from the FC to auditory cortex (AC) influencing dynamic sensory filters (Caras and Sanes, 2017; Bimbard et al., 2018; Schneider et al., 2018; Winkowski et al., 2018; Mittelstadt and Kanold, 2023; Macedo-Lima et al., 2024), we wondered whether the differential receptive plasticity was driven by distinct FC representations of the two opposite behavioral paradigms.
Therefore, we trained two groups of ferrets on two opposite auditory categorical Go-NoGo paradigms, requiring each group to discriminate noncompact sound categories (Yin et al., 2016, 2020). Task stimuli varied along two acoustic feature dimensions: spectral frequency (TN-task) or temporal modulation rate (amplitude-modulated white noise, AM-task). As indicated above, in the P-paradigm group, ferrets learned to lick for water reward when Target stimuli were presented and refrained from licking to Reference stimuli. In contrast, the group that learned the N-paradigm performed the opposite behavior and refrained from licking for water when Target stimuli were presented but could lick freely to Reference sounds (Fig. 1 A).
