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Visualizing stimulus convergence in amygdala neurons during associative learning.

ABSTRACT: A central feature of models of associative memory formation is the reliance on information convergence from pathways responsive to the conditioned stimulus (CS) and unconditioned stimulus (US). In particular, cells receiving coincident input are held to be critical for subsequent plasticity. Yet identification of neurons in the mammalian brain that respond to such coincident inputs during a learning event remains elusive. Here we use Arc cellular compartmental analysis of temporal gene transcription by fluorescence in situ hybridization (catFISH) to locate populations of neurons in the mammalian brain that respond to both the CS and US during training in a one-trial learning task, conditioned taste aversion (CTA). Individual neurons in the basolateral nucleus of the amygdala (BLA) responded to both the CS taste and US drug during conditioning. Coincident activation was not evident, however, when stimulus exposure was altered so as to be ineffective in promoting learning (backward conditioning, latent inhibition). Together, these data provide clear visualization of neurons in the mammalian brain receiving convergent information about the CS and US during acquisition of a learned association.

SUBMITTER: Barot SK

PROVIDER: S-EPMC2634890 | biostudies-other | 2008 Dec

REPOSITORIES: biostudies-other

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Visualizing stimulus convergence in amygdala neurons during associative learning.

Barot Sabiha K SK Kyono Yasuhiro Y Clark Emily W EW Bernstein Ilene L IL

Proceedings of the National Academy of Sciences of the United States of America 20081217 52

A central feature of models of associative memory formation is the reliance on information convergence from pathways responsive to the conditioned stimulus (CS) and unconditioned stimulus (US). In particular, cells receiving coincident input are held to be critical for subsequent plasticity. Yet identification of neurons in the mammalian brain that respond to such coincident inputs during a learning event remains elusive. Here we use Arc cellular compartmental analysis of temporal gene transcrip ...[more]

PMID: 19091953

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Project description:BackgroundAssociative conditioning is a ubiquitous form of learning throughout the animal kingdom and fear conditioning is one of the most widely researched models for studying its neurobiological basis. Fear conditioning is also considered a model system for understanding phobias and anxiety disorders. A fundamental issue in fear conditioning regards the existence and location of neurons in the brain that receive convergent information about the conditioned stimulus (CS) and unconditioned stimulus (US) during the acquisition of conditioned fear memory. Convergent activation of neurons is generally viewed as a key event for fear learning, yet there has been almost no direct evidence of this critical event in the mammalian brain.Methodology/principal findingsHere, we used Arc cellular compartmental analysis of temporal gene transcription by fluorescence in situ hybridization (catFISH) to identify neurons activated during single trial contextual fear conditioning in rats. To conform to temporal requirements of catFISH analysis we used a novel delayed contextual fear conditioning protocol which yields significant single- trial fear conditioning with temporal parameters amenable to catFISH analysis. Analysis yielded clear evidence that a population of BLA neurons receives convergent CS and US information at the time of the learning, that this only occurs when the CS-US arrangement is supportive of the learning, and that this process requires N-methyl-D-aspartate receptor activation. In contrast, CS-US convergence was not observed in dorsal hippocampus.Conclusions/significanceBased on the pattern of Arc activation seen in conditioning and control groups, we propose that a key requirement for CS-US convergence onto BLA neurons is the potentiation of US responding by prior exposure to a novel CS. Our results also support the view that contextual fear memories are encoded in the amygdala and that the role of dorsal hippocampus is to process and transmit contextual CS information.

Project description:Orbitofrontal cortex (OFC), medial frontal cortex (MFC), and amygdala mediate stimulus-reward learning, but the mechanisms through which they interact are unclear. Here, we investigated how neurons in macaque OFC and MFC signaled rewards and the stimuli that predicted them during learning with and without amygdala input. Macaques performed a task that required them to evaluate two stimuli and then choose one to receive the reward associated with that option. Four main findings emerged. First, amygdala lesions slowed the acquisition and use of stimulus-reward associations. Further analyses indicated that this impairment was due, at least in part, to ineffective use of negative feedback to guide subsequent decisions. Second, the activity of neurons in OFC and MFC rapidly evolved to encode the amount of reward associated with each stimulus. Third, amygdalectomy reduced encoding of stimulus-reward associations during the evaluation of different stimuli. Reward encoding of anticipated and received reward after choices were made was not altered. Fourth, amygdala lesions led to an increase in the proportion of neurons in MFC, but not OFC, that encoded the instrumental response that monkeys made on each trial. These correlated changes in behavior and neural activity after amygdala lesions strongly suggest that the amygdala contributes to the ability to learn stimulus-reward associations rapidly by shaping encoding within OFC and MFC.SIGNIFICANCE STATEMENT Altered functional interactions among orbital frontal cortex (OFC), medial frontal cortex (MFC), and amygdala are thought to underlie several psychiatric conditions, many related to reward learning. Here, we investigated the causal contribution of the amygdala to the development of neuronal activity in macaque OFC and MFC related to rewards and the stimuli that predict them during learning. Without amygdala inputs, neurons in both OFC and MFC showed decreased encoding of stimulus-reward associations. MFC also showed increased encoding of the instrumental responses that monkeys made on each trial. Behaviorally, changes in neural activity were accompanied by slower stimulus-reward learning. The findings suggest that interactions among amygdala, OFC, and MFC contribute to learning about stimuli that predict rewards.

Dataset Information

Visualizing stimulus convergence in amygdala neurons during associative learning.

Publications

Visualizing stimulus convergence in amygdala neurons during associative learning.

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