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Context-Dependent Odor Learning Requires the Anterior Olfactory Nucleus
Learning to associate the context in which a stimulus occurs is an important aspect of animal learning. We propose that the association of an olfactory stimulus with its multisensory context is mediated by projections from ventral hippocampus (vHC) networks to the anterior olfactory nucleus (AON). U...
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Published in: | Behavioral neuroscience 2020-08, Vol.134 (4), p.332-343 |
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container_title | Behavioral neuroscience |
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creator | Levinson, Max Kolenda, Jacob P. Alexandrou, Gabriella J. Escanilla, Olga Cleland, Thomas A. Smith, David M. Linster, Christiane |
description | Learning to associate the context in which a stimulus occurs is an important aspect of animal learning. We propose that the association of an olfactory stimulus with its multisensory context is mediated by projections from ventral hippocampus (vHC) networks to the anterior olfactory nucleus (AON). Using a contextually cued olfactory discrimination task, rats were trained to associate 2 olfactory stimuli with different responses depending on visuospatial context. Temporary lesions of the AON or vHC impaired performance on this task. In contrast, such lesions did not impair performance on a noncontextual olfactory discrimination task. Moreover, vHC lesions also impaired performance on an analogous contextually cued texture discrimination task, whereas AON lesions affected only olfactory contextual associations. We describe a distinct role for the AON in olfactory processing and conclude that early olfactory networks such as the olfactory bulb and AON function as multimodal integration networks rather than processing olfactory signals exclusively. |
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We propose that the association of an olfactory stimulus with its multisensory context is mediated by projections from ventral hippocampus (vHC) networks to the anterior olfactory nucleus (AON). Using a contextually cued olfactory discrimination task, rats were trained to associate 2 olfactory stimuli with different responses depending on visuospatial context. Temporary lesions of the AON or vHC impaired performance on this task. In contrast, such lesions did not impair performance on a noncontextual olfactory discrimination task. Moreover, vHC lesions also impaired performance on an analogous contextually cued texture discrimination task, whereas AON lesions affected only olfactory contextual associations. 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We propose that the association of an olfactory stimulus with its multisensory context is mediated by projections from ventral hippocampus (vHC) networks to the anterior olfactory nucleus (AON). Using a contextually cued olfactory discrimination task, rats were trained to associate 2 olfactory stimuli with different responses depending on visuospatial context. Temporary lesions of the AON or vHC impaired performance on this task. In contrast, such lesions did not impair performance on a noncontextual olfactory discrimination task. Moreover, vHC lesions also impaired performance on an analogous contextually cued texture discrimination task, whereas AON lesions affected only olfactory contextual associations. 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Kolenda, Jacob P. ; Alexandrou, Gabriella J. ; Escanilla, Olga ; Cleland, Thomas A. ; Smith, David M. ; Linster, Christiane</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a471t-ff104ee75fcfbb39604e1f4df6a2ddd71153a0c8425a62cf2b58c7da767d96e83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animal</topic><topic>Animal behavior</topic><topic>Animal Learning</topic><topic>Animals</topic><topic>Brain - physiology</topic><topic>Brain Lesions (Experimental)</topic><topic>Cerebral Cortex - physiology</topic><topic>Contextual Associations</topic><topic>Cues</topic><topic>Discrimination Learning</topic><topic>Hippocampus</topic><topic>Hippocampus - physiology</topic><topic>Information processing</topic><topic>Learning - physiology</topic><topic>Lesions</topic><topic>Male</topic><topic>Odorants</topic><topic>Olfaction</topic><topic>Olfactory bulb</topic><topic>Olfactory Bulb - physiology</topic><topic>Olfactory Cortex - metabolism</topic><topic>Olfactory Cortex - physiology</topic><topic>Olfactory discrimination learning</topic><topic>Olfactory Pathways - physiology</topic><topic>Olfactory Perception</topic><topic>Olfactory Perception - physiology</topic><topic>Olfactory Stimulation</topic><topic>Olfactory stimuli</topic><topic>Rats</topic><topic>Rats, Long-Evans</topic><topic>Sensory integration</topic><topic>Smell</topic><topic>Smell - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Levinson, Max</creatorcontrib><creatorcontrib>Kolenda, Jacob P.</creatorcontrib><creatorcontrib>Alexandrou, Gabriella J.</creatorcontrib><creatorcontrib>Escanilla, Olga</creatorcontrib><creatorcontrib>Cleland, Thomas A.</creatorcontrib><creatorcontrib>Smith, David M.</creatorcontrib><creatorcontrib>Linster, Christiane</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>PsycARTICLES</collection><collection>ProQuest One Psychology</collection><collection>Animal Behavior Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Behavioral neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Levinson, Max</au><au>Kolenda, Jacob P.</au><au>Alexandrou, Gabriella J.</au><au>Escanilla, Olga</au><au>Cleland, Thomas A.</au><au>Smith, David M.</au><au>Linster, Christiane</au><au>Schoenbaum, Geoffrey</au><au>Burwell, Rebecca D</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Context-Dependent Odor Learning Requires the Anterior Olfactory Nucleus</atitle><jtitle>Behavioral neuroscience</jtitle><addtitle>Behav Neurosci</addtitle><date>2020-08-01</date><risdate>2020</risdate><volume>134</volume><issue>4</issue><spage>332</spage><epage>343</epage><pages>332-343</pages><issn>0735-7044</issn><issn>1939-0084</issn><eissn>1939-0084</eissn><abstract>Learning to associate the context in which a stimulus occurs is an important aspect of animal learning. We propose that the association of an olfactory stimulus with its multisensory context is mediated by projections from ventral hippocampus (vHC) networks to the anterior olfactory nucleus (AON). Using a contextually cued olfactory discrimination task, rats were trained to associate 2 olfactory stimuli with different responses depending on visuospatial context. Temporary lesions of the AON or vHC impaired performance on this task. In contrast, such lesions did not impair performance on a noncontextual olfactory discrimination task. Moreover, vHC lesions also impaired performance on an analogous contextually cued texture discrimination task, whereas AON lesions affected only olfactory contextual associations. 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subjects | Animal Animal behavior Animal Learning Animals Brain - physiology Brain Lesions (Experimental) Cerebral Cortex - physiology Contextual Associations Cues Discrimination Learning Hippocampus Hippocampus - physiology Information processing Learning - physiology Lesions Male Odorants Olfaction Olfactory bulb Olfactory Bulb - physiology Olfactory Cortex - metabolism Olfactory Cortex - physiology Olfactory discrimination learning Olfactory Pathways - physiology Olfactory Perception Olfactory Perception - physiology Olfactory Stimulation Olfactory stimuli Rats Rats, Long-Evans Sensory integration Smell Smell - physiology |
title | Context-Dependent Odor Learning Requires the Anterior Olfactory Nucleus |
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