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Amygdala Neurons Differentially Encode Motivation and Reinforcement
Open accessAbstract
Lesion studies demonstrate that the basolateral amygdala complex (BLA) is important for assigning motivational significance to sensory stimuli, but little is known about how this information is encoded. We used in vivo electrophysiology procedures to investigate how the amygdala encodes motivating and reinforcing properties of cues that induce reinstatement of reward-seeking behavior. Two groups of rats were trained to respond to a sucrose reward. The “paired” group was trained with a reward-predictive cue, whereas the “unpaired” group was trained with a randomly presented cue. Both groups underwent identical extinction and reinstatement procedures during which the reward was withheld. The proportion of neurons that were phasically cue responsive during reinstatement was significantly higher in the paired group (46 of 100) than in the unpaired group (8 of 112). Cues that induce reward-seeking behavior can do so by acting as incentives or reinforcers. Distinct populations of neurons responded to the cue in trials in which the cue acted as an incentive, triggering a motivated reward-seeking state, or as a reinforcer, supporting continued instrumental responding. The incentive motivation-encoding population of neurons (34 of 46 cue-responsive neurons; 74%) extinguished in temporal agreement with a decrease in the rate of instrumental responding. The conditioned reinforcement-encoding population of neurons (12 of 46 cue-responsive neurons; 26%) maintained their response for the duration of cue-reinforced instrumental responding. These data demonstrate that separate populations of cue-responsive neurons in the BLA encode the motivating or reinforcing properties of a cue previously associated with a reward.
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“In this way, cues predicting threat are themselves recognized as threatening60 and, likewise, those predicting reward themselves become rewarding61,62.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [61]
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“…orbitofrontal cortex (OFC), which is reciprocally connected to the BLA (Kita and Kitai, 1990; Shi and Cassell, 1998), is thought to work in coordination with the BLA to use incentive information to guide behavior (Gallagher and Schoenbaum, 1999; Schoenbaum et al., 1999, 2003; Baxter et al., 2000).”
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“The orbitofrontal cortex (OFC), which is reciprocally connected to the BLA (Kita and Kitai, 1990; Shi and Cassell, 1998), is thought to work in coordination with the BLA to use incentive information to guide behavior (Gallagher and Schoenbaum, 1999; Schoenbaum et al., 1999, 2003; Baxter et al.,…”
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“Evidence suggests that the mPFC regulates the responsiveness of BLA neurons to odor cues previously associated with footshock (Rosenkranz et al., 2003).”
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“…that the BLA is a site for the neural representation of reward-associated cues that induce reinstatement to reward-seeking behavior, consistent with studies showing that the BLA is critically involved in cue-induced reinstatement (Meil and See, 1997; Fuchs and See, 2002; Yun and Fields, 2003).”
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“Studies have shown that pyramidal neurons and interneurons can be differentiated by both morphological and electrophysiological characteristics (Washburn and Moises, 1992; Rainnie et al., 1993).”
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“…stimulus that acquires reinforcing properties when associated with primary reinforcement, and conditioned reinforcement can be measured by the ability of the cue to support instrumental responding in the absence of the primary reinforcer (Arroyo et al., 1998; Everitt and Robbins, 2000, 2005).”
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“Rats readily lever press to self-administer primary reinforcers, such as sucrose, cocaine, or alcohol, and subsequently to obtain reward-paired cues in the absence of reward (Davis and Smith 1976; Meil and See 1997; Grimm et al. 2002; Nie and Janak, 2003).”
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“…bursts per second, and percentage of total spikes that occur in bursts in the BLA neurons of the paired group as compared with the unpaired group (Table 2) suggest that the reward-paired cue may induce bursting of BLA neurons and are consistent with the study done by Laviolette et al. (2005).”
BackgroundResultRapid Associative Encoding in Basolateral Amygdala Depends on Connections with Orbitofrontal Cortex
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“It has been shown that lesions of either the BLA or OFC alter the neural encoding of information about expected outcomes and acquired value (Schoenbaum et al., 2003; Saddoris et al., 2005).”
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“…that the BLA is a site for the neural representation of reward-associated cues that induce reinstatement to reward-seeking behavior, consistent with studies showing that the BLA is critically involved in cue-induced reinstatement (Meil and See, 1997; Fuchs and See, 2002; Yun and Fields, 2003).”
ResultIntracellular recordings from morphologically identified neurons of the basolateral amygdala
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“Studies have shown that pyramidal neurons and interneurons can be differentiated by both morphological and electrophysiological characteristics (Washburn and Moises, 1992; Rainnie et al., 1993).”
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BackgroundInfluentialNeuronal organization of the lateral and basolateral amygdaloid nuclei in the rat
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“Electrophysiological characterization of neuronal response types Pyramidal projection neurons compose 95% of the neurons in the BLA, the remainder being interneurons (McDonald 1982, 1984).”
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“In addition, the BLA sends inputs to the nucleus accumbens core (Kelley et al., 1982; Wright et al., 1996), and it has been reported that these connections are important for performing second-order conditioned responses (Setlow et al., 2002).”
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Conditioned craving and arousal in cocaine addiction: a preliminary report.
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“Rats readily lever press to self-administer primary reinforcers, such as sucrose, cocaine, or alcohol, and subsequently to obtain reward-paired cues in the absence of reward (Davis and Smith 1976; Meil and See 1997; Grimm et al. 2002; Nie and Janak, 2003).”
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“Rats readily lever press to self-administer primary reinforcers, such as sucrose, cocaine, or alcohol, and subsequently to obtain reward-paired cues in the absence of reward (Davis and Smith 1976; Meil and See 1997; Grimm et al. 2002; Nie and Janak, 2003).”
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“…that the BLA is a site for the neural representation of reward-associated cues that induce reinstatement to reward-seeking behavior, consistent with studies showing that the BLA is critically involved in cue-induced reinstatement (Meil and See, 1997; Fuchs and See, 2002; Yun and Fields, 2003).”
ResultFunctions of the Amygdala and Related Forebrain Areas in Attention and Cognition
Gallagher, M., & Schoenbaum, G. M. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09279.x · Cited by 64 · cited 2×
“…orbitofrontal cortex (OFC), which is reciprocally connected to the BLA (Kita and Kitai, 1990; Shi and Cassell, 1998), is thought to work in coordination with the BLA to use incentive information to guide behavior (Gallagher and Schoenbaum, 1999; Schoenbaum et al., 1999, 2003; Baxter et al., 2000).”
BackgroundThe amygdala and associative learning
Gallagher, M. (2000) · doi:10.1093/oso/9780198505013.003.0008 · Cited by 24
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Metadata
- Authors
- Tye, K. M., & Janak, P. H.
- Affiliations
- University of California, San Francisco (US)
- Corresponding author
- Janak, Patricia H.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2007-04-11
- Volume
- 27
- Issue
- 15
- Pages
- 3937-3945
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6672525
- OpenAlex
- W2076741191
- Cited by
- 130
- References
- 50
- Citations by year
- 2026: 5 · 2025: 8 · 2024: 8 · 2023: 5 · 2022: 10 · 2021: 8 · 2020: 3 · 2019: 3 · 2017: 15 · 2016: 5 · 2015: 11 · 2014: 6 · 2013: 7 · 2012: 6
- FWCI
- 3.84
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- basolateral amygdala, motivation, reinforcement, incentive motivation, conditioned reinforcement, reinstatement, extinction, reward-seeking behavior, sucrose reward, instrumental responding, neural coding
- MeSH terms
- Action Potentials, Amygdala, Animals, Male, Motivation, Neurons, Reinforcement, Psychology, Reward, Rats, Sprague-Dawley, Rats
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