Cargando…

Multisensory integration of orally‐sourced gustatory and olfactory inputs to the posterior piriform cortex in awake rats

ABSTRACT: Flavour refers to the sensory experience of food, which is a combination of sensory inputs sourced from multiple modalities during consumption, including taste and odour. Previous work has demonstrated that orally‐sourced taste and odour cues interact to determine perceptual judgements of...

Descripción completa

Detalles Bibliográficos
Autores principales: Idris, Ammar, Christensen, Brooke A., Walker, Ellen M., Maier, Joost X.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9869978/
https://www.ncbi.nlm.nih.gov/pubmed/36385245
http://dx.doi.org/10.1113/JP283873
_version_ 1784876879932555264
author Idris, Ammar
Christensen, Brooke A.
Walker, Ellen M.
Maier, Joost X.
author_facet Idris, Ammar
Christensen, Brooke A.
Walker, Ellen M.
Maier, Joost X.
author_sort Idris, Ammar
collection PubMed
description ABSTRACT: Flavour refers to the sensory experience of food, which is a combination of sensory inputs sourced from multiple modalities during consumption, including taste and odour. Previous work has demonstrated that orally‐sourced taste and odour cues interact to determine perceptual judgements of flavour stimuli, although the underlying cellular‐ and circuit‐level neural mechanisms remain unknown. We recently identified a region of the piriform olfactory cortex in rats that responds to both taste and odour stimuli. Here, we investigated how converging taste and odour inputs to this area interact to affect single neuron responsiveness ensemble coding of flavour identity. To accomplish this, we recorded spiking activity from ensembles of single neurons in the posterior piriform cortex (pPC) in awake, tasting rats while delivering taste solutions, odour solutions and taste + odour mixtures directly into the oral cavity. Our results show that taste and odour inputs evoke highly selective, temporally‐overlapping responses in multisensory pPC neurons. Comparing responses to mixtures and their unisensory components revealed that taste and odour inputs interact in a non‐linear manner to produce unique response patterns. Taste input enhances trial‐by‐trial decoding of odour identity from small ensembles of simultaneously recorded neurons. Together, these results demonstrate that taste and odour inputs to pPC interact in complex, non‐linear ways to form amodal flavour representations that enhance identity coding. [Image: see text] KEY POINTS: Experience of food involves taste and smell, although how information from these different senses is combined by the brain to create our sense of flavour remains unknown. We recorded from small groups of neurons in the olfactory cortex of awake rats while they consumed taste solutions, odour solutions and taste + odour mixtures. Taste and smell solutions evoke highly selective responses. When presented in a mixture, taste and smell inputs interacted to alter responses, resulting in activation of unique sets of neurons that could not be predicted by the component responses. Synergistic interactions increase discriminability of odour representations. The olfactory cortex uses taste and smell to create new information representing multisensory flavour identity.
format Online
Article
Text
id pubmed-9869978
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher John Wiley and Sons Inc.
record_format MEDLINE/PubMed
spelling pubmed-98699782023-01-23 Multisensory integration of orally‐sourced gustatory and olfactory inputs to the posterior piriform cortex in awake rats Idris, Ammar Christensen, Brooke A. Walker, Ellen M. Maier, Joost X. J Physiol Neuroscience ABSTRACT: Flavour refers to the sensory experience of food, which is a combination of sensory inputs sourced from multiple modalities during consumption, including taste and odour. Previous work has demonstrated that orally‐sourced taste and odour cues interact to determine perceptual judgements of flavour stimuli, although the underlying cellular‐ and circuit‐level neural mechanisms remain unknown. We recently identified a region of the piriform olfactory cortex in rats that responds to both taste and odour stimuli. Here, we investigated how converging taste and odour inputs to this area interact to affect single neuron responsiveness ensemble coding of flavour identity. To accomplish this, we recorded spiking activity from ensembles of single neurons in the posterior piriform cortex (pPC) in awake, tasting rats while delivering taste solutions, odour solutions and taste + odour mixtures directly into the oral cavity. Our results show that taste and odour inputs evoke highly selective, temporally‐overlapping responses in multisensory pPC neurons. Comparing responses to mixtures and their unisensory components revealed that taste and odour inputs interact in a non‐linear manner to produce unique response patterns. Taste input enhances trial‐by‐trial decoding of odour identity from small ensembles of simultaneously recorded neurons. Together, these results demonstrate that taste and odour inputs to pPC interact in complex, non‐linear ways to form amodal flavour representations that enhance identity coding. [Image: see text] KEY POINTS: Experience of food involves taste and smell, although how information from these different senses is combined by the brain to create our sense of flavour remains unknown. We recorded from small groups of neurons in the olfactory cortex of awake rats while they consumed taste solutions, odour solutions and taste + odour mixtures. Taste and smell solutions evoke highly selective responses. When presented in a mixture, taste and smell inputs interacted to alter responses, resulting in activation of unique sets of neurons that could not be predicted by the component responses. Synergistic interactions increase discriminability of odour representations. The olfactory cortex uses taste and smell to create new information representing multisensory flavour identity. John Wiley and Sons Inc. 2022-12-05 2023-01-01 /pmc/articles/PMC9869978/ /pubmed/36385245 http://dx.doi.org/10.1113/JP283873 Text en © 2022 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Neuroscience
Idris, Ammar
Christensen, Brooke A.
Walker, Ellen M.
Maier, Joost X.
Multisensory integration of orally‐sourced gustatory and olfactory inputs to the posterior piriform cortex in awake rats
title Multisensory integration of orally‐sourced gustatory and olfactory inputs to the posterior piriform cortex in awake rats
title_full Multisensory integration of orally‐sourced gustatory and olfactory inputs to the posterior piriform cortex in awake rats
title_fullStr Multisensory integration of orally‐sourced gustatory and olfactory inputs to the posterior piriform cortex in awake rats
title_full_unstemmed Multisensory integration of orally‐sourced gustatory and olfactory inputs to the posterior piriform cortex in awake rats
title_short Multisensory integration of orally‐sourced gustatory and olfactory inputs to the posterior piriform cortex in awake rats
title_sort multisensory integration of orally‐sourced gustatory and olfactory inputs to the posterior piriform cortex in awake rats
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9869978/
https://www.ncbi.nlm.nih.gov/pubmed/36385245
http://dx.doi.org/10.1113/JP283873
work_keys_str_mv AT idrisammar multisensoryintegrationoforallysourcedgustatoryandolfactoryinputstotheposteriorpiriformcortexinawakerats
AT christensenbrookea multisensoryintegrationoforallysourcedgustatoryandolfactoryinputstotheposteriorpiriformcortexinawakerats
AT walkerellenm multisensoryintegrationoforallysourcedgustatoryandolfactoryinputstotheposteriorpiriformcortexinawakerats
AT maierjoostx multisensoryintegrationoforallysourcedgustatoryandolfactoryinputstotheposteriorpiriformcortexinawakerats