Role of Amygdalo-Nigral Circuitry in Conditioning of a Visual Stimulus Paired with Food

Lee, Hongjoo J.; Groshek, Frank; Petrovich, Gorica D.; Cantalini, Joseph P.; Gallagher, Michela; Holland, Peter C.

doi:10.1523/jneurosci.0416-05.2005

Cited by 103 publications

(132 citation statements)

References 40 publications

(39 reference statements)

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“…Disconnection of the CeA and SNc prevented the normal acquisition of conditioned orienting to a visual cue paired with food (Lee et al, 2005). In the same study, the authors showed that the medial CeA cells retrogradely labeled from the SNc expressed an immediate-early gene, FOS, after conditioned orienting responses, demonstrating the direct involvement of the CeA to SNc projection in conditioned orienting.…”

Section: Discussionmentioning

confidence: 86%

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Role of Substantia Nigra–Amygdala Connections in Surprise-Induced Enhancement of Attention

Lee¹,

Youn²,

O³

et al. 2006

J. Neurosci.

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Coding of prediction error by midbrain dopamine neurons has been examined extensively in the framework of associative learning theory. Most of this research has focused on the role of prediction error in determining the reinforcement value of unconditioned stimuli: poorly predicted ("surprising") outcomes are more effective reinforcers and produce a greater dopamine response than well predicted outcomes. However, surprise also enhances attention to cues that signal poorly predicted outcomes. Previous reports from our laboratories demonstrated that circuitry, including the amygdala central nucleus (CeA), the cholinergic neurons of the substantia innominata/ nucleus basalis region, and their innervation of the posterior parietal cortex, is critical to these surprise-induced enhancements of attention in associative learning. The present study considered the origin of prediction error information important for the operation of this system by examining the effects of disrupting communication between the midbrain substantia nigra pars compacta (SNc) and the CeA. Rats received unilateral lesions of the SNc and lesions of the CeA in either the contralateral or ipsilateral hemisphere. Contralateral lesions eliminated the surprise-induced enhancement of attention and learning that was displayed by rats with ipsilateral control lesions. These results show that SNc-CeA communication is critical to mechanisms by which the coding of prediction error by midbrain dopamine neurons is translated into enhancement of attention and learning modulated by the cholinergic system.

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Section: Discussionmentioning

confidence: 86%

“…A second series of sections was used for tyrosine hydroxylase (TH) immunoreactivity, to evaluate the lesions made to SNc DA cells. The assessment of TH immunoreactivity followed a standard immunohistochemical protocol for free-floating tissues (Lee et al, 2005).…”

Section: Methodsmentioning

confidence: 99%

Role of Substantia Nigra–Amygdala Connections in Surprise-Induced Enhancement of Attention

Lee¹,

Youn²,

O³

et al. 2006

J. Neurosci.

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“…However, we did find the habenula to be functionally coupled with the amygdala, which has reciprocal connections with the substantia nigra (25). The substantia nigra is the main output of the LHb (5) and plays a crucial role in associative learning.…”

Section: Discussionmentioning

confidence: 92%

The habenula encodes negative motivational value associated with primary punishment in humans

Lawson

Seymour

Loh

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

126

110

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Learning what to approach, and what to avoid, involves assigning value to environmental cues that predict positive and negative events. Studies in animals indicate that the lateral habenula encodes the previously learned negative motivational value of stimuli. However, involvement of the habenula in dynamic trialby-trial aversive learning has not been assessed, and the functional role of this structure in humans remains poorly characterized, in part, due to its small size. Using high-resolution functional neuroimaging and computational modeling of reinforcement learning, we demonstrate positive habenula responses to the dynamically changing values of cues signaling painful electric shocks, which predict behavioral suppression of responses to those cues across individuals. By contrast, negative habenula responses to monetary reward cue values predict behavioral invigoration. Our findings show that the habenula plays a key role in an online aversive learning system and in generating associated motivated behavior in humans.high-resolution fMRI | conditioned behavior | pallidum L earning which stimuli predict positive and negative outcomes, and thus should be approached or avoided, respectively, is central to an organism's ability to survive. Midbrain dopamine neurons respond to both unpredicted rewarding stimuli and to cues previously paired with rewards (1), consistent with behavioral approach toward those cues. As a counterpoint to these reward-related signals, neurons in the lateral habenula (LHb) of nonhuman primates respond to previously learned stimuli predicting the delivery of punishments and the omission of rewards, whereas they are inhibited by stimuli that signal upcoming rewards (2). These studies in nonhuman primates have concentrated on well-learned stimuli, and so have forsaken the opportunity to study the details of dynamic adaptation in the habenula. However, in many real-world scenarios, organisms learn about the motivational value of novel cues in their environment gradually, one exposure at a time, which raises the question as to whether the habenula plays a role in encoding the dynamically changing motivational value of cues that predict negative events.Dynamic learning from aversive events permits the rapid experience-dependent updating of behavior, for example, the automatic suppression of approach, which is a characteristic of aversive conditioning (3). The LHb receives inputs from the globus pallidus (4), and its excitation inhibits midbrain dopamine neurons via the rostromedial tegmental nucleus (2). This position as a hub between corticolimbic networks and midbrain monoaminergic nuclei provides a means through which positively or negatively valenced stimuli can modulate motor output, leading to the hypothesis that the habenula plays a critical role in motivated behavior (5).Studies using temporally precise optogenetic stimulation of the LHb in rodents provide convincing evidence that the habenula drives behavioral suppression (6). This structure has been suggested as a novel target for de...

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“…Although our data suggest that both the BLA and CeN likely use valence-independent neuronal circuits to produce changes in arousal, they may affect physiological, attentional, behavioral, and mnemonic processes differently via their distinct sets of efferent projections (47). For example, projections from the CeN to the substantia nigra may be important for conditioned orienting responses (48), whereas projections from the BLA through the stria terminalis may be important for modulation of some forms of positively and negatively valenced memories (5). It is also possible that projections from the BLA to the CeN coordinate or permit changes in aspects of emotional arousal (49).…”

Section: Discussionmentioning

confidence: 99%

Substantial similarity in amygdala neuronal activity during conditioned appetitive and aversive emotional arousal

Shabel

Janak

2009

Proc. Natl. Acad. Sci. U.S.A.

182

136

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The amygdala is important for determining the emotional significance of environmental stimuli. However, the degree to which appetitive and aversive stimuli are processed by the same or different neuronal circuits within the amygdala remains unclear. Here we show that neuronal activity during the expression of classically conditioned appetitive and aversive emotional responses is more similar than expected by chance, despite the different sensory modalities of the eliciting stimuli. We also found that the activity of a large number of cells (> 43%) was correlated with blood pressure, a measure of emotional arousal. Together, our results suggest that a substantial proportion of neuronal circuits within the amygdala can contribute to both appetitive and aversive emotional arousal.autonomic ͉ electrophysiology ͉ emotion ͉ fear ͉ Pavlovian conditioning

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Role of Amygdalo-Nigral Circuitry in Conditioning of a Visual Stimulus Paired with Food

Cited by 103 publications

References 40 publications

Role of Substantia Nigra–Amygdala Connections in Surprise-Induced Enhancement of Attention

Role of Substantia Nigra–Amygdala Connections in Surprise-Induced Enhancement of Attention

The habenula encodes negative motivational value associated with primary punishment in humans

Substantial similarity in amygdala neuronal activity during conditioned appetitive and aversive emotional arousal

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