The higher order auditory cortex is involved in the assignment of affective value to sensory stimuli

Abstract

The sensory cortex participates in emotional memory but its role is poorly understood. Here we show that inactivation of the higher order auditory cortex Te2 in rats during early memory consolidation impairs remote first- and second-order fear memories but not the association between two neutral cues. Furthermore, Te2 inactivation prevents changes in the valence of such information. Following the presentation of two auditory cues previously paired with either pleasant or painful stimuli, a large percentage of cells responds to both experiences but also a small fraction of neurons responds exclusively to one of them. The latter type of neurons signals the valence rather than the salience or the motor responses associated with the stimuli, and reflects selective associative processes. Pharmacogenetic silencing of memory-activated neurons causes amnesia. Thus, Te2 represents a crucial node for the assignment of the affective value to sensory stimuli and for the storage of such information.

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

“…In support of this notion, we have identified higher order components of sensory cortices, such as the temporal auditory cortex Te2, which are essential for storing remote fearful memories (Cambiaghi et al 2015;Grosso et al 2015b;Sacco and Sacchetti 2010).…”

“…Thus, the auditory cortex may be part of a sensorimotor system that links auditory stimuli to specific motor responses and, therefore, the differences detected in the present study between fear vs. appetitive paradigms may be due to such the different motor responses paired to tones. Because our recent study showed that Te2 activity in the layer II/III is not related to these motor processes 15 (Grosso et al 2015b), it may be that other Te2 layers are recruited by these sensorimotor processes, and specifically the layer V which projects to subcortical structures involved in emotional and motor responses regulation (Paxinos, 2004). To address this issue, we performed zif268 analysis in rats trained to associate an auditory CS to a different motor behaviors, i.e.…”

“…To address this issue, we performed zif268 analysis in rats trained to associate an auditory CS to a different motor behaviors, i.e. an active avoidance reaction (Grosso et al 2015b). In these rats, during memory retention test, the presentation of the CS determined an escape conditioned reaction to the adjacent chamber (n = 6) which is not present in naive rats (n = 8) (t12= 0.76; p < 0.01) (Fig.…”

“…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. Nevertheless, a comprehensive picture of the circuits that are engaged by emotional associative processes within the auditory cortex of mammals is still lacking.…”

“…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).…”