Associatively learned representations of taste outcomes activate taste-encoding neural ensembles in gustatory cortex

Michael P. Saddoris, Peter C Holland, Michela Gallagher

Research output: Contribution to journalArticle

Abstract

Through learning processes, cues associated with emotionally salient reinforcing outcomes can come to act as substitutes for the reinforcer itself. According to one account of this phenomenon, the predictive cue associatively elicits a representation of the expected outcome by reactivating cells responsible for encoding features of the primary reinforcer.Wetested this hypothesis by examining the role of neural ensembles in gustatory cortex (GC) during receipt of gustatory stimuli (sucrose and water) and cues associated with those stimuli using the immediate early genes (IEGs) Arc and Homer1a. Because these plasticity-related IEGs are expressed in the neuronal nucleus 5 and 30 min, respectively, after salient events, we examined how individual neurons encoded these stimuli in two separate behavioral epochs. In experiment 1, we showed that tasting identical sucrose solutions, but not tasteless water, in the two epochs increased both IEG activity and the degree of overlap between neural ensembles in GC. In experiment 2, odor cues associated with sucrose, but not water, evoked potentiation of IEG activity in GC similar to sucrose itself. Surprisingly, lesions of the basolateral amygdala had minimal effects on associative encoding in GC. Finally, these associatively driven representations of sucrose appeared to be outcome specific, as neural ensembles that were activated by the sucrose-associated cue were also activated by sucrose itself. This degree of overlap between associative and primary taste activity at the ensemble level suggests that GC neurons encode important information about anticipated outcomes. Such representations may provide outcome-specific information for guiding goal-directed behavior.

Original languageEnglish (US)
Pages (from-to)15386-15396
Number of pages11
JournalJournal of Neuroscience
Volume29
Issue number49
DOIs
StatePublished - Dec 9 2009

Fingerprint

Sucrose
Immediate-Early Genes
Cues
Water
Neurons
Learning

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Associatively learned representations of taste outcomes activate taste-encoding neural ensembles in gustatory cortex. / Saddoris, Michael P.; Holland, Peter C; Gallagher, Michela.

In: Journal of Neuroscience, Vol. 29, No. 49, 09.12.2009, p. 15386-15396.

Research output: Contribution to journalArticle

@article{b5434aaa190b46a8ab64cf664e49e22f,
title = "Associatively learned representations of taste outcomes activate taste-encoding neural ensembles in gustatory cortex",
abstract = "Through learning processes, cues associated with emotionally salient reinforcing outcomes can come to act as substitutes for the reinforcer itself. According to one account of this phenomenon, the predictive cue associatively elicits a representation of the expected outcome by reactivating cells responsible for encoding features of the primary reinforcer.Wetested this hypothesis by examining the role of neural ensembles in gustatory cortex (GC) during receipt of gustatory stimuli (sucrose and water) and cues associated with those stimuli using the immediate early genes (IEGs) Arc and Homer1a. Because these plasticity-related IEGs are expressed in the neuronal nucleus 5 and 30 min, respectively, after salient events, we examined how individual neurons encoded these stimuli in two separate behavioral epochs. In experiment 1, we showed that tasting identical sucrose solutions, but not tasteless water, in the two epochs increased both IEG activity and the degree of overlap between neural ensembles in GC. In experiment 2, odor cues associated with sucrose, but not water, evoked potentiation of IEG activity in GC similar to sucrose itself. Surprisingly, lesions of the basolateral amygdala had minimal effects on associative encoding in GC. Finally, these associatively driven representations of sucrose appeared to be outcome specific, as neural ensembles that were activated by the sucrose-associated cue were also activated by sucrose itself. This degree of overlap between associative and primary taste activity at the ensemble level suggests that GC neurons encode important information about anticipated outcomes. Such representations may provide outcome-specific information for guiding goal-directed behavior.",
author = "Saddoris, {Michael P.} and Holland, {Peter C} and Michela Gallagher",
year = "2009",
month = "12",
day = "9",
doi = "10.1523/JNEUROSCI.3233-09.2009",
language = "English (US)",
volume = "29",
pages = "15386--15396",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "49",

}

TY - JOUR

T1 - Associatively learned representations of taste outcomes activate taste-encoding neural ensembles in gustatory cortex

AU - Saddoris, Michael P.

AU - Holland, Peter C

AU - Gallagher, Michela

PY - 2009/12/9

Y1 - 2009/12/9

N2 - Through learning processes, cues associated with emotionally salient reinforcing outcomes can come to act as substitutes for the reinforcer itself. According to one account of this phenomenon, the predictive cue associatively elicits a representation of the expected outcome by reactivating cells responsible for encoding features of the primary reinforcer.Wetested this hypothesis by examining the role of neural ensembles in gustatory cortex (GC) during receipt of gustatory stimuli (sucrose and water) and cues associated with those stimuli using the immediate early genes (IEGs) Arc and Homer1a. Because these plasticity-related IEGs are expressed in the neuronal nucleus 5 and 30 min, respectively, after salient events, we examined how individual neurons encoded these stimuli in two separate behavioral epochs. In experiment 1, we showed that tasting identical sucrose solutions, but not tasteless water, in the two epochs increased both IEG activity and the degree of overlap between neural ensembles in GC. In experiment 2, odor cues associated with sucrose, but not water, evoked potentiation of IEG activity in GC similar to sucrose itself. Surprisingly, lesions of the basolateral amygdala had minimal effects on associative encoding in GC. Finally, these associatively driven representations of sucrose appeared to be outcome specific, as neural ensembles that were activated by the sucrose-associated cue were also activated by sucrose itself. This degree of overlap between associative and primary taste activity at the ensemble level suggests that GC neurons encode important information about anticipated outcomes. Such representations may provide outcome-specific information for guiding goal-directed behavior.

AB - Through learning processes, cues associated with emotionally salient reinforcing outcomes can come to act as substitutes for the reinforcer itself. According to one account of this phenomenon, the predictive cue associatively elicits a representation of the expected outcome by reactivating cells responsible for encoding features of the primary reinforcer.Wetested this hypothesis by examining the role of neural ensembles in gustatory cortex (GC) during receipt of gustatory stimuli (sucrose and water) and cues associated with those stimuli using the immediate early genes (IEGs) Arc and Homer1a. Because these plasticity-related IEGs are expressed in the neuronal nucleus 5 and 30 min, respectively, after salient events, we examined how individual neurons encoded these stimuli in two separate behavioral epochs. In experiment 1, we showed that tasting identical sucrose solutions, but not tasteless water, in the two epochs increased both IEG activity and the degree of overlap between neural ensembles in GC. In experiment 2, odor cues associated with sucrose, but not water, evoked potentiation of IEG activity in GC similar to sucrose itself. Surprisingly, lesions of the basolateral amygdala had minimal effects on associative encoding in GC. Finally, these associatively driven representations of sucrose appeared to be outcome specific, as neural ensembles that were activated by the sucrose-associated cue were also activated by sucrose itself. This degree of overlap between associative and primary taste activity at the ensemble level suggests that GC neurons encode important information about anticipated outcomes. Such representations may provide outcome-specific information for guiding goal-directed behavior.

UR - http://www.scopus.com/inward/record.url?scp=71849115069&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=71849115069&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.3233-09.2009

DO - 10.1523/JNEUROSCI.3233-09.2009

M3 - Article

VL - 29

SP - 15386

EP - 15396

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 49

ER -