Higher-Order Sensory Cortex Drives Basolateral Amygdala Activity during the Recall of Remote, but Not Recently Learned Fearful Memories

Abstract

Negative experiences are quickly learned and long remembered. Key unresolved issues in the field of emotional memory include identifying the loci and dynamics of memory storage and retrieval. The present study examined neural activity in the higher-order auditory cortex Te2 and basolateral amygdala (BLA) and their crosstalk during the recall of recent and remote fear memories. To this end, we obtained local field potentials and multiunit activity recordings in Te2 and BLA of rats that underwent recall at 24 h and 30 d after the association of an acoustic conditioned (CS, tone) and an aversive unconditioned stimulus (US, electric shock). Here we show that, during the recall of remote auditory threat memories in rats, the activity of the Te2 and BLA is highly synchronized in the theta frequency range. This functional connectivity stems from memory consolidation processes because it is present during remote, but not recent, memory retrieval. Moreover, the observed increase in synchrony is cue and region specific. A preponderant Te2-to-BLA directionality characterizes this dialogue, and the percentage of time Te2 theta leads the BLA during remote memory recall correlates with a faster latency to freeze to the auditory conditioned stimulus. The blockade of this information transfer via Te2 inhibition with muscimol prevents any retrieval-evoked neuronal activity in the BLA and animals are unable to retrieve remote memories. We conclude that memories stored in higher-order sensory cortices drive BLA activity when distinguishing between learned threatening and neutral stimuli.

Experience-Dependent Coding of Time-Dependent Frequency Trajectories by Off Responses in Secondary Auditory Cortex

“…At a more detailed circuit level though, since A2 receives input both from core auditory cortex (Covic and Sherman, 2011) as well as the dorsal division of the medial geniculate (Llano and Sherman, 2008), which exhibits traditional offset responses (He, 2001;Anderson and Linden, 2016), it remains to be seen whether the site of plasticity underlying the emergence of more A2 Off responses after maternal experience lies within auditory cortex or at the thalamic level. Nevertheless, by responding to more pup-like frequency trajectories after pup care experience, the maternal A2 may help create a neural representation that is more tolerant of variability in natural call trajectories, so that presumed downstream limbic areas like the amygdala (LeDoux et al, 1991;Cambiaghi et al, 2016) can more categorically drive subcortical circuits for maternal responsiveness (Banerjee and Liu, 2013). Perhaps in a similar way, intonation differences between emotionally distinct sounds (Banziger and Scherer, 2005;Zatorre and Baum, 2012) may also be processed through A2 to generate intrinsic or learned physiological responses.…”

Experience-dependent coding of frequency-modulated trajectories by offsets in auditory cortex

“…Primate secondary auditory cortex can also exhibit more categorical responses to trained sound categories [65], and is thought to lie along a hierarchical pathway that produces progressively more categorical responses [66]. By responding to more pup-like frequency trajectories after pup care experience, the maternal A2 may help create a neural representation that is more tolerant of variability in natural call trajectories, so that presumed downstream limbic areas like the amygdala [67,68] can more categorically drive subcortical circuits for maternal responsiveness [69]. Perhaps in a similar way, intonation differences between emotionally distinct sounds [4,39] may also be processed through A2 to generate intrinsic or learned physiological responses.…”

Fronto-Temporal Coupling Dynamics During Spontaneous Activity and Auditory Processing in the Bat Carollia perspicillata

“…Several studies have pinpointed an involvement of low-frequency synchronization in the functional coupling between the frontal cortex and a variety of brain structures. Coherent oscillations between distant cortical areas (including the frontal cortex) in the low-frequency range correlate with working memory (Daume et al, 2017), fear memory consolidation (Popa et al, 2010), attentional selection (Womelsdorf and Everling, 2015), and long-term fear recall (Cambiaghi et al, 2016;Karalis et al, 2016). In the auditory domain, top-down control exerted from frontal cortical areas, through low-frequency oscillatory activity, increases coupling to speech signals in the human AC (Park et al, 2015).…”