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

ABSTRACT 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.
    Cell 07/2015; 162(1):134-145. DOI:10.1016/j.cell.2015.06.027 · 32.24 Impact Factor
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    • "x appeared to get input from a random assortment of mitral / tufted cells . Thus RABV tracing was able to identify that each of the three different efferent projection sites appeared to have a different representation of the olfactory map than the one present in the olfactory bulb , a finding supported by other studies ( Stettler and Axel , 2009 ; Choi et al . , 2011 ; Sosulski et al . , 2011 ) . These represent only a few examples of the many studies that have used RABV to map connectivity in different circuits throughout the central nervous system ( Yonehara et al . , 2011 ; Sun et al . , 2014 ) as well as the spinal cord ( Stepien et al . , 2010 ; Tripodi et al . , 2011 ; Esposito et al . , 2014 "
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    ABSTRACT: The nervous system is complex not simply because of the enormous number of neurons it contains but by virtue of the specificity with which they are connected. Unraveling this specificity is the task of neuroanatomy. In this endeavor, neuroanatomists have traditionally exploited an impressive array of tools ranging from the Golgi method to electron microscopy. An ideal method for studying anatomy would label neurons that are interconnected, and, in addition, allow expression of foreign genes in these neurons. Fortuitously, nature has already partially developed such a method in the form of neurotropic viruses, which have evolved to deliver their genetic material between synaptically connected neurons while largely eluding glia and the immune system. While these characteristics make some of these viruses a threat to human health, simple modifications allow them to be used in controlled experimental settings, thus enabling neuroanatomists to trace multi-synaptic connections within and across brain regions. Wild-type neurotropic viruses, such as rabies and alpha-herpes virus, have already contributed greatly to our understanding of brain connectivity, and modern molecular techniques have enabled the construction of recombinant forms of these and other viruses. These newly engineered reagents are particularly useful, as they can target genetically defined populations of neurons, spread only one synapse to either inputs or outputs, and carry instructions by which the targeted neurons can be made to express exogenous proteins, such as calcium sensors or light-sensitive ion channels, that can be used to study neuronal function. In this review, we address these uniquely powerful features of the viruses already in the neuroanatomist's toolbox, as well as the aspects of their biology that currently limit their utility. Based on the latter, we consider strategies for improving viral tracing methods by reducing toxicity, improving control of transsynaptic spread, and extending t
    Frontiers in Neuroanatomy 05/2015; 9:80. DOI:10.3389/fnana.2015.00080 · 3.54 Impact Factor
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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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    ABSTRACT: How memories are formed and stored in the brain remains a fascinating question in neuroscience. Here we discuss the memory engram theory, our recent attempt to identify and manipulate memory engram cells in the brain with optogenetics, and how these methods are used to address questions such as how false memory is formed and how the valence of a memory can be changed in the brain. Copyright © 2014 Cold Spring Harbor Laboratory Press; all rights reserved.
    Cold Spring Harbor Symposia on Quantitative Biology 01/2015; 79. DOI:10.1101/sqb.2014.79.024901
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