Rapid Spectrotemporal Plasticity in Primary Auditory Cortex during Behavior

Abstract

Complex natural and environmental sounds, such as speech and music, convey information along both spectral and temporal dimensions. The cortical representation of such stimuli rapidly adapts when animals become actively engaged in discriminating them. In this study, we examine the nature of these changes using simplified spectrotemporal versions (upward vs downward shifting tone sequences) with domestic ferrets (Mustela putorius). Cortical processing rapidly adapted to enhance the contrast between the two discriminated stimulus categories, by changing spectrotemporal receptive field properties to encode both the spectral and temporal structure of the tone sequences. Furthermore, the valence of the changes was closely linked to the task reward structure: stimuli associated with negative reward became enhanced relative to those associated with positive reward. These task-and-stimulus-related spectrotemporal receptive field changes occurred only in trained animals during, and immediately following, behavior. This plasticity was independently confirmed by parallel changes in a directionality function measured from the responses to the transition of tone sequences during task performance. The results demonstrate that induced patterns of rapid plasticity reflect closely the spectrotemporal structure of the task stimuli, thus extending the functional relevance of rapid task-related plasticity to the perception and learning of natural sounds such speech and animal vocalizations.

Region- and Layer-Specific Activation of the Higher Order Auditory Cortex Te2 after Remote Retrieval of Fear or Appetitive Memories

“…Similar results were reported by Bao et al (Bao et al 2001), who showed that, after pairing of auditory stimuli presentation to ventral tegmental area stimulation, "strong, sharply tuned responses to the paired tones also emerge in a second cortical area [Te2], whereas the same stimuli only evoke 23 poor or non-selective responses in this second cortical field in naive animals." Furthermore, beside Te2, several recent studies showed that also the neurons in the primary auditory cortex Te1 undergo profound and selective changes during either appetitive and aversive learning tasks (David et al 2012;Fritz et al 2005a;Yin et al 2014). Remarkably, the valence of these changes was strictly linked to the task reward structure, rather than to peripheral motor responses (David et al 2012;Fritz et al 2005a;Yin et al 2014), in line with our present data.…”

“…Furthermore, beside Te2, several recent studies showed that also the neurons in the primary auditory cortex Te1 undergo profound and selective changes during either appetitive and aversive learning tasks (David et al 2012;Fritz et al 2005a;Yin et al 2014). Remarkably, the valence of these changes was strictly linked to the task reward structure, rather than to peripheral motor responses (David et al 2012;Fritz et al 2005a;Yin et al 2014), in line with our present data. Thus, the present study, together with past research, supports the view that the activity of the auditory cortex is profoundly influenced by the emotional information assigned to sensory stimuli and raises the intriguing possibility that learned emotional value is a property of stimulus representation in the sensory cortex.…”

“…Intriguingly, many studies have shown that the learned emotional-motivational charge of sounds shapes the activity of neurons in the primary (Bieszczad and Weinberger 2012;David et al 2012;Letzkus et al 2011;Pi et al 2013;Yin et al 2014) and higher order (Bao et al 2001;Carretta et al 1999;Kown et al 2012;Grosso et al 2015b;Sacco and Sacchetti 2010) auditory cortex. For example, it has been shown that the emotional content provided by similar auditory stimuli, but paired to either an aversive or an appetitive stimulus, was able to shape the plasticity of the auditory cortical receptive field in opposite ways (David et al 2012;Yin et al 2014).…”

“…For example, it has been shown that the emotional content provided by similar auditory stimuli, but paired to either an aversive or an appetitive stimulus, was able to shape the plasticity of the auditory cortical receptive field in opposite ways (David et al 2012;Yin et al 2014). Taken together, these findings suggest that associative and motivational processes are pronounced within the auditory cortex, where they can help to link the physical attributes of the stimuli to the affective charge or to the behavioral responses occurring during emotional experiences (Cambiaghi et al 2016;Grosso et al 2015aGrosso et al , 2015b.…”

Top-down modulation of sensory cortex gates perceptual learning

“…This result is in line with an abundance of work demonstrating behaviorally gated modulations of ACx activity (37,(44)(45)(46)(47)(48)(49)(62)(63)(64)(65)(66). Our observation that disengaged neural sensitivity is better if measured immediately after behavioral testing, rather than before (compare green lines in Fig.…”