Context-dependent odor learning requires the anterior olfactory nucleus.

Levinson, Max; Kolenda, Jacob P.; Alexandrou, Gabriella; Escanilla, Olga; Cleland, Thomas A.; Smith, David M.; Linster, Christiane

doi:10.1037/bne0000371

Cited by 27 publications

(24 citation statements)

References 41 publications

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“…Neurons in the middle of the spectrum with dual odor- and spatial-selectivity, presumably receiving converging bottom-up and top-down information, are well-positioned to connect transient sensory cues to spatial goals during navigation. Future studies on the distinct functions of aPCx and pPCx, as well as subregions of olfactory cortex outside of piriform cortex such as the anterior olfactory nucleus or cortical amydala 23, 32, 33, 51, 54, 55 will undoubtedly contribute to a more comprehensive understanding of integration of olfactory and spatial information, and the distinct roles of neural pathways engaged during odor-guided spatial behaviors.…”

Section: Discussionmentioning

confidence: 99%

Spatial maps in piriform cortex during olfactory navigation

Poo

Agarwal

Bonacchi

et al. 2020

Preprint

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Animals rely on chemical signals to forage for food, shelter, and mates. Such behaviors call for odor cues to be linked to locations within their environment . Nonetheless, where and how this happens in the brain is not known. Here, we show that spatial and olfactory information converge in posterior piriform cortex (pPCx), an olfactory region with strong associative circuity.Ensembles of pPCx neurons recorded in rats performing an odor-cued spatial navigation task were robustly selective for both odor identity and spatial location, forming an "odor-place map".Spatially-selective pPCx neurons displayed joint selectivity for odors, stability across behavioral contexts and functional coupling to the hippocampal theta rhythm. These results implicate the pPCx as a strong candidate region to associate spatial and olfactory information in support of navigational behavior. Main Text:Navigation requires the flexible integration of sensory information with a cognitive map of the environment ( 1 ) . The hippocampal formation and the primary olfactory (piriform) cortex (PCx) are believed to be dedicated to spatial navigation and olfactory discrimination, respectively ( 2 -8 ) . PCx neurons receive direct sensory input from olfactory bulb (OB) projection neurons ( 9 , 10 ) , but also contain dense recurrent olfactory circuitry and receive long-range corticocortical input from regions including the frontal cortex and temporal lobe ( 11 , 12 ) , including the hippocampus and the lateral entorhinal cortex (LEC) ( 12 -15 ) . C omputational modeling suggests that PCx neural architecture is well-suited to perform associative functions ( 16 -18 ) , which is supported by evidence for odor recognition and memory in PCx ( 19 -22 ) .While these properties of PCx make it a strong candidate to associate odor and spatial information, there is yet no physiological evidence for spatial representations here. To investigate, we developed a novel odor-cued spatial task that challenged rats to use spatial information along with odor identity to navigate to a specific location for reward. We recorded from the posterior PCx (pPCx) and area CA1 of the hippocampus in rats performing this task.We focused on pPCx due to the relative preponderance of associative circuits and connectivity to higher-order regions that have been found there ( 12 , 21 -24 ) . Our behavioral arena consisted of an elevated plus-maze with a 1 square meter footprint that was positioned in a room with visual landmarks ( Fig. 1A and supplementary video ). At the end of each arm was a port, each of which could deliver either an odor stimulus or a water reward.Trials began when an LED was activated at one of the four ports. If the rat inserted its snout into the lighted port, it received one of four odors chosen at random. Each odor could be presented at any one of the four possible initiation ports and, no matter where it was presented, it indicated a fixed reward location (e.g. odor 1 the north, odor 2 to the south, etc.) ( Fig. 1A, B ).After sampling the odor, the animal cou...

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Section: Discussionmentioning

confidence: 99%

Spatial maps in piriform cortex during olfactory navigation

Poo

Agarwal

Bonacchi

et al. 2020

Preprint

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“…Several discrete pulses in evolution of piriform cortex size can be traced in the fossil record (below), and this evidence is consistent with its division into anatomically distinct anterior and posterior parts. The anterior olfactory nucleus (now considered a part of the anterior piriform cortex) is also involved (Brunjes et al, 2005;Levinson et al, 2020). Here we will focus on the olfactory cortex, the part of piriform cortex receiving direct input from the mitral and tufted cells of the olfactory bulb.…”

Section: Piriform Cortex Contains Different Areasmentioning

confidence: 99%

An Evolutionary Microcircuit Approach to the Neural Basis of High Dimensional Sensory Processing in Olfaction

Shepherd

Rowe

Greer

2021

Front. Cell. Neurosci.

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Odor stimuli consist of thousands of possible molecules, each molecule with many different properties, each property a dimension of the stimulus. Processing these high dimensional stimuli would appear to require many stages in the brain to reach odor perception, yet, in mammals, after the sensory receptors this is accomplished through only two regions, the olfactory bulb and olfactory cortex. We take a first step toward a fundamental understanding by identifying the sequence of local operations carried out by microcircuits in the pathway. Parallel research provided strong evidence that processed odor information is spatial representations of odor molecules that constitute odor images in the olfactory bulb and odor objects in olfactory cortex. Paleontology provides a unique advantage with evolutionary insights providing evidence that the basic architecture of the olfactory pathway almost from the start ∼330 million years ago (mya) has included an overwhelming input from olfactory sensory neurons combined with a large olfactory bulb and olfactory cortex to process that input, driven by olfactory receptor gene duplications. We identify a sequence of over 20 microcircuits that are involved, and expand on results of research on several microcircuits that give the best insights thus far into the nature of the high dimensional processing.

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“…Odor-discrimination learning is supported by the hippocampus and relies on both higher-order and primary sensory cortices (Martin et al 2007). Higher-order areas, such as the ventral hippocampus, exhibit direct projections to the AON, whereby top-down input by the hippocampus on AON modulates the processing of incoming olfactory information, especially in regard to contextual processing and stored internal representations (Aqrabawi and Kim 2018;Levinson et al 2020). In this manner, the AON may act as a central hub between olfactory input and odor memory (Oettl et al 2016;Linster and Kelsch 2019;Aqrabawi and Kim 2020).…”

Section: Grin1mentioning

confidence: 99%

Genetic influences of autism candidate genes on circuit wiring and olfactory decoding

et al. 2021

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Olfaction supports a multitude of behaviors vital for social communication and interactions between conspecifics. Intact sensory processing is contingent upon proper circuit wiring. Disturbances in genetic factors controlling circuit assembly and synaptic wiring can lead to neurodevelopmental disorders, such as autism spectrum disorder (ASD), where impaired social interactions and communication are core symptoms. The variability in behavioral phenotype expression is also contingent upon the role environmental factors play in defining genetic expression. Considering the prevailing clinical diagnosis of ASD, research on therapeutic targets for autism is essential. Behavioral impairments may be identified along a range of increasingly complex social tasks. Hence, the assessment of social behavior and communication is progressing towards more ethologically relevant tasks. Garnering a more accurate understanding of social processing deficits in the sensory domain may greatly contribute to the development of therapeutic targets. With that framework, studies have found a viable link between social behaviors, circuit wiring, and altered neuronal coding related to the processing of salient social stimuli. Here, the relationship between social odor processing in rodents and humans is examined in the context of health and ASD, with special consideration for how genetic expression and neuronal connectivity may regulate behavioral phenotypes.

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Context-dependent odor learning requires the anterior olfactory nucleus.

Cited by 27 publications

References 41 publications

Spatial maps in piriform cortex during olfactory navigation

Spatial maps in piriform cortex during olfactory navigation

An Evolutionary Microcircuit Approach to the Neural Basis of High Dimensional Sensory Processing in Olfaction

Genetic influences of autism candidate genes on circuit wiring and olfactory decoding

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