Driving Opposing Behaviors with Ensembles of Piriform Neurons

Department of Neuroscience and the Howard Hughes Medical Institute, College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA.
Cell (Impact Factor: 32.24). 09/2011; 146(6):1004-15. DOI: 10.1016/j.cell.2011.07.041
Source: PubMed


Anatomic and physiologic studies have suggested a model in which neurons of the piriform cortex receive convergent input from random collections of glomeruli. In this model, odor representations can only be afforded behavioral significance upon experience. We have devised an experimental strategy that permits us to ask whether the activation of an arbitrarily chosen subpopulation of neurons in piriform cortex can elicit different behavioral responses dependent upon learning. Activation of a small subpopulation of piriform neurons expressing channelrhodopsin at multiple loci in the piriform cortex, when paired with reward or shock, elicits either appetitive or aversive behavior. Moreover, we demonstrate that different subpopulations of piriform neurons expressing ChR2 can be discriminated and independently entrained to elicit distinct behaviors. These observations demonstrate that the piriform cortex is sufficient to elicit learned behavioral outputs in the absence of sensory input. These data imply that the piriform does not use spatial order to map odorant identity or behavioral output.

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    • "We have also shown that an olfactory CS connects to US representations in the BLA to generate learned behavior, indicating that olfactory conditioning may utilize the same circuit mechanisms as those proposed for auditory fear conditioning. In olfaction , each odor activates a distinct ensemble of neurons in piriform cortex, and each unique ensemble is capable of serving as a CS (Choi et al., 2011; Illig and Haberly, 2003; Rennaker et al., 2007; Stettler and Axel, 2009). Piriform cortex projects directly to the BLA (Luskin and Price, 1983; Schwabe et al., 2004), and we demonstrate that a US representation in the BLA is essential for the expression of learned olfactory behavior. "
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    ABSTRACT: Stimuli that possess inherently rewarding or aversive qualities elicit emotional responses and also induce learning by imparting valence upon neutral sensory cues. Evidence has accumulated implicating the amygdala as a critical structure in mediating these processes. We have developed a genetic strategy to identify the representations of rewarding and aversive unconditioned stimuli (USs) in the basolateral amygdala (BLA) and have examined their role in innate and learned responses. Activation of an ensemble of US-responsive cells in the BLA elicits innate physiological and behavioral responses of different valence. Activation of this US ensemble can also reinforce appetitive and aversive learning when paired with differing neutral stimuli. Moreover, we establish that the activation of US-responsive cells in the BLA is necessary for the expression of a conditioned response. Neural representations of conditioned and unconditioned stimuli therefore ultimately connect to US-responsive cells in the BLA to elicit both innate and learned responses. Copyright © 2015 Elsevier Inc. All rights reserved.
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    • "For instance, Johansen et al. (2010) showed that optically activated lateral amygdala (LA) cells were sufficient to substitute as a US during tone (CS) presentations and, upon subsequent tone presentations , animals displayed fear behavior despite the CS and US having never been naturally, or exogenously, presented. Another study showed that an activated population of pyriform cortex neurons, when paired with rewards or shocks, could drive the associated appetitive or aversive behavioral output upon stimulation of the same neurons (Choi et al. 2011). Moreover, pairing footshocks with optogenetically reactivated secondary auditory cortex and medial geniculate nucleus (MGN) inputs to the LA was also sufficient to form an associative fear memory to the optically activated terminals (Kwon et al. 2014). "
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    • "Figure 3 shows habituation data from 12 MO Tg2576 and WT mice (n = 12 each). In rodents, short-term odor habituation is a behavioral read-out of piriform cortical function [39], [40], as is, in part, behavioral odor discrimination [29], [31], [41]. The single-unit sensory physiology results described above suggest that there may be intact odor discrimination in Tg2576 mice compared to WT. "
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