Optogenetic Stimulation of Lateral Amygdala Input to Posterior Piriform Cortex Modulates Single-Unit and Ensemble Odor Processing

Abstract

Olfactory information is synthesized within the olfactory cortex to provide not only an odor percept, but also a contextual significance that supports appropriate behavioral response to specific odor cues. The piriform cortex serves as a communication hub within this circuit by sharing reciprocal connectivity with higher processing regions, such as the lateral entorhinal cortex and amygdala. The functional significance of these descending inputs on piriform cortical processing of odorants is currently not well understood. We have employed optogenetic methods to selectively stimulate lateral and basolateral amygdala (BLA) afferent fibers innervating the posterior piriform cortex (pPCX) to quantify BLA modulation of pPCX odor-evoked activity. Single unit odor-evoked activity of anesthetized BLA-infected animals was significantly modulated compared with control animal recordings, with individual cells displaying either enhancement or suppression of odor-driven spiking. In addition, BLA activation induced a decorrelation of odor-evoked pPCX ensemble activity relative to odor alone. Together these results indicate a modulatory role in pPCX odor processing for the BLA complex. This interaction could contribute to learned changes in PCX activity following associative conditioning, as well as support alternate patterns of odor processing that are state-dependent.

Cue-induced reinstatement of alcohol-seeking behavior is associated with increased CaMKII T286 phosphorylation in the reward pathway of mice

“…The piriform is part of the olfactory cortex and plays a critical role in odor memory (Wilson and Stevenson, 2003) and odor cue-reward processing (Truchet et al, 2002). The piriform functions as an association cortex and has strong connections with the amygdala, which play a key role in linking odors with emotional or motivational value (Sadrian and Wilson, 2015). Prior research has shown that odor cue-induced reinstatement of alcohol-seeking behavior was associated with increased Fos expression in the piriform cortex of rats (Jupp et al, 2011).…”

“…Under these conditions, exposure to the small volume of alcohol may have provided sufficient olfactory stimulation to increase pCaMKII-T286 IR in the piriform directly or through odor-based memory processing. Alternatively, the BLA sends CaMKII-positive glutamatergic projections to the piriform, allowing the amygdala to modulate odor processing (Luna and Morozov, 2012; Majak et al, 2004; Sadrian and Wilson, 2015). Thus, the concomitant increase in pCaMKII-T286 IR in the BLA and piriform may indicate circuit activation induced by interactive processing of the compound cue and CaMKII-dependent processing of alcohol reinforcement in the amygdala (e.g., (Salling et al, 2016)).…”

Development of Odor Hedonics: Experience-Dependent Ontogeny of Circuits Supporting Maternal and Predator Odor Responses in Rats

“…Furthermore, learned aversive and appetitive odors differentially activate rat anterior (aPCX) and posterior (pPCX) piriform cortex (Moriceau and Sullivan, 2004b;Xia et al, 2015) and human PCX Li et al, 2006). These hedonically modulated responses within the primary sensory pathway may reflect either intrinsic coding properties of olfactory pathway neurons for appetitive and aversive odors and/or interaction between the sensory pathway and limbic circuits (Sadrian and Wilson, 2015). For example, in addition to primary sensory areas, odors varying in hedonic valence are differentially encoded by activity within the amygdala, OFC, and other regions (Schoenbaum et al, 1999;Anderson et al, 2003;Root et al, 2014;Jin et al, 2015;Patin and Pause, 2015).…”

Encoding of odor fear memories in the mouse olfactory cortex

“…Piriform cortex has long been hypothesized to support auto-associative network functions that can retrieve previously learned information from partial or degraded sensory inputs (Haberly, 2001;Wilson and Sullivan, 2011). Piriform pyramidal cells form a large recurrent network, which is reciprocally connected with adjacent highorder associative areas including the prefrontal, entorhinal and perirhinal cortex and the amygdala (Johnson et al, 2000;Sadrian and Wilson, 2015). Storage of information is made possible by NMDA-dependent, associative plasticity of connections (Johenning et al, 2009;Kanter and Haberly, 1990;Quinlan et al, 2004).…”