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

Abstract

The auditory cortex is involved in encoding sounds which have acquired an emotional-motivational charge. However, the neural circuitry engaged by emotional memory processes in the auditory cortex is poorly understood. In this study, we investigated the layers and regions that are recruited in the higher order auditory cortex Te2 by a tone previously paired to either fear or appetitive stimuli in rats. By tracking the protein coded by the immediate early gene zif268, we found that fear memory retrieval engages layers II-III in most regions of Te2. These results were neither due to an enhanced fear state nor to fear-evoked motor responses, as they were absent in animals retrieving an olfactory fear memory. These layers were also activated by appetitive auditory memory retrieval. Strikingly, layer IV was recruited by fear, but not appetitive memories, whereas layer V activity was related to the behavioral responses displayed to the CS.In addition to revealing the layers and regions which are recruited in the Te2 by either fear or appetitive remote memories, our study also shows that the neural circuitry within the Te2 that processes and stores emotional memories varies on the basis of the affective-motivational charge of tones.

Human olfactory cortex contributes to emotional and perceptual aspects of aversive associative learning and memory

“…Also coinciding animal findings, this CS-specific odor retuning arose only on Day 9, indicating a time-dependent process likely involved in the transformation of associative learning into long-term memory (Weinberger, 2004). Moreover, the site of this retuning-the PPC, a secondary olfactory cortex-conformed to animal findings, emphasizing conditioning-induced plasticity and long-term memory storage in the secondary sensory cortex (relative to primary or higher sensory levels; Diamond and Weinberger, 1984;Grosso et al, 2015bGrosso et al, , 2017Holschneider et al, 2006;Poremba et al, 1998). The timing (Day 9 only) and site (PPC only) of tuning shifts paralleled changes in higher-order, spatially distributed neuronal ensemble responses in the PPC (i.e., biased PPC classification to the threat CS on Day 9).…”

“…Animal evidence further suggests that this associative plasticity in the sensory cortex not only emerges immediately after conditioning but also shows long-term retention with growing specificity to the CS (Weinberger, 2004). Importantly, associative plasticity in the secondary sensory cortex, both immediate and long-lasting, plays a critical role in threat memory, with the immediate plasticity being necessary for the formation (Cambiaghi et al, 2016a;Grosso et al, 2015b;Yang et al, 2016) and the lasting plasticity necessary for the long-term storage (Cambiaghi et al, 2016b;Grosso et al, 2015bGrosso et al, , 2017Kwon et al, 2012;Sacco and Sacchetti, 2010) of threat memory.…”

Reversible Inactivation of the Higher Order Auditory Cortex during Fear Memory Consolidation Prevents Memory-Related Activity in the Basolateral Amygdala during Remote Memory Retrieval

“…To better address this issue, we employed an alternative method based on the expression of the immediate early gene zif268. Immediate early genes are required for synaptic plasticity and are used as an index of neuronal activation (Frankland and Bontempi, 2005; Sacco and Sacchetti, 2010; Lesburguères et al, 2011; Kwon et al, 2012; Grosso et al, 2017). Among immediate-early genes, zif268 expression has been associated with long-term plasticity that occurs during memory retrieval (Frankland et al, 2004; Kwon et al, 2012; Xie et al, 2014; Grosso et al, 2017).…”

“…Immediate early genes are required for synaptic plasticity and are used as an index of neuronal activation (Frankland and Bontempi, 2005; Sacco and Sacchetti, 2010; Lesburguères et al, 2011; Kwon et al, 2012; Grosso et al, 2017). Among immediate-early genes, zif268 expression has been associated with long-term plasticity that occurs during memory retrieval (Frankland et al, 2004; Kwon et al, 2012; Xie et al, 2014; Grosso et al, 2017). Accordingly, several recent studies have shown changes in zif268 expression in the sensory cortex following emotional memory recall (Hall et al, 2001; Maviel et al, 2004; Sacco and Sacchetti, 2010; Kwon et al, 2012).…”

“…In fact, previous studies have shown that the retrieval of fearful memories engages all cortical layers (Cho et al, 2016; Grosso et al, 2017). In particular, by measuring zif268 expression after the recall of fearful memories, layers 2 and 3 showed the wider increment across the entire extension of the Te2 (Grosso et al, 2017), in line with the idea that these superficial laminae are recruited by associative processes (Frankland et al, 2004; Maviel et al, 2004; Lesburguères et al, 2011). Furthermore, in Te2 superficial layers, we discovered “associative value-coding” neurons whose activity signals the affective value assigned to auditory stimuli (Grosso et al, 2015b).…”