Amygdalo-striatal interaction in the enhancement of stimulus salience in associative learning.

Esber, Guillem R.; Torres-Tristani, Karina; Holland, Peter C.

doi:10.1037/bne0000041

Cited by 10 publications

(11 citation statements)

References 44 publications

(71 reference statements)

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“…Conveniently, in most cases, we found that rats with ipsilateral damage were unimpaired. We found that lesions that disconnected CeA from SNc (Lee et al, 2006), SI (Han et al, 1999), or DLS (Esber et al, 2015) all abolished the shift advantage found in ipsilateral controls, without producing differences in performance in the consistent condition. By contrast, Wheeler et al (2014) found that both contralateral and ipsilateral lesions of CeA and LH, as well as unilateral lesions of LH alone, eliminated the shift advantage, suggesting that LH’s influence on salience enhancement did not depend on any privileged convergence of information processing by CeA and LH.…”

Section: Surprise-induced Increases In Associabilitymentioning

confidence: 73%

Mini-review: Prediction errors, attention and associative learning

Holland

Schiffino

2016

Neurobiology of Learning and Memory

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Most modern theories of associative learning emphasize a critical role for prediction error (PE, the difference between received and expected events). One class of theories, exemplified by the Rescorla-Wagner (1972) model, asserts that PE determines the effectiveness of the reinforcer or unconditioned stimulus (US): surprising reinforcers are more effective than expected ones. A second class, represented by the Pearce-Hall (1980) model, argues that PE determines the associability of conditioned stimuli (CSs), the rate at which they may enter into new learning: the surprising delivery or omission of a reinforcer enhances subsequent processing of the CSs that were present when PE was induced. In this mini-review we describe evidence, mostly from our laboratory, for PE-induced changes in the associability of both CSs and USs, and the brain systems involved in the coding, storage and retrieval of these altered associability values. This evidence favors a number of modifications to behavioral models of how PE influences event processing, and suggests the involvement of widespread brain systems in animals’ responses to PE.

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Section: Surprise-induced Increases In Associabilitymentioning

confidence: 73%

Mini-review: Prediction errors, attention and associative learning

Holland

Schiffino

2016

Neurobiology of Learning and Memory

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“…Thus, the excitotoxic lesions of DLS did not appear to damage SNc or its dopaminergic innervation of DLS. Although this analysis was conducted on only a subset of rats in experiment 1, its results are consistent with those of a more extensive analysis after identical lesions in another study (Esber et al ., ).…”

Section: Resultsmentioning

confidence: 97%

“…Rats with ipsilateral lesions of CeA and SNc showed normal conditioned ORs (Lee et al ., ) and normal associability enhancements in the serial prediction task (Lee et al ., ), but rats with contralateral lesions of those structures did not. Similarly, we found that contralateral lesions of CeA and DLS disrupted both conditioned ORs (Han et al ., ) and surprise‐induced associability enhancements (Esber et al ., ).…”

Section: Discussionmentioning

confidence: 97%

“…Reig & Silberberg, ) is further tempered by Esber et al . 's () observation that rats with unilateral lesions of DLS contralateral to CeA lesions failed to show associability enhancements. Although, because of their CeA lesions, rats in that study may have coded altered cue associability information in PPC unilaterally, that information could nevertheless be made available to both hemispheres of DLS, because many cortical neurons project to dorsal striatum bilaterally (e.g.…”

Section: Discussionmentioning

confidence: 99%

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Dorsolateral striatum is critical for the expression of surprise‐induced enhancements in cue associability

Asem

Schiffino

Holland

2015

Eur J of Neuroscience

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The dorsolateral striatum (DLS) is frequently implicated in sensory-motor integration, including the performance of sensory orienting responses and learned stimulus-response habits. Our laboratory previously identified a role for the DLS in rats' performance of conditioned orienting responses (ORs) to Pavlovian cues for food delivery. Here, we considered whether DLS is also critical to another aspect of attention in associative learning, the surprise-induced enhancement of cue associability. A large behavioral literature shows that a cue present when an expected event is omitted enters into new associations more rapidly, when that cue is subsequently paired with food. Research from our laboratory has shown that both cue associability enhancements and conditioned ORs depend on the function of a circuit that includes the amygdala central nucleus and the substantia nigra pars compacta. In three experiments, we explored the involvement of DLS in surprise-induced associability enhancements, using a three-stage serial prediction task that permitted separation of DLS function in registering surprise (prediction error) and enhancing cue associability, and in using that increased associability to learn more rapidly about that cue later. The results showed that DLS is critical to the expression, but not the establishment, of the enhanced cue associability normally produced by surprise in this task. They extend the role of DLS and the amygdalo-nigro-striatal circuit underlying learned orienting to more subtle aspects of attention in associative learning, but are consistent with the general notion that DLS is more important in the expression of previously-acquired tendencies than in their acquisition.

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“…While the neural encoding of such changes has long been attributed to the amygdala (Esber et al, 2015; Madarasz et al, 2016; Peck and Salzman, 2014; Sears et al, 2014; Stillman et al, 2015; Tye et al, 2008), emerging evidence suggests that the paraventricular nucleus of the thalamus (PVT) contributes to the regulation of emotional responses (Haight and Flagel, 2014; Hsu et al, 2014; Kirouac, 2015). PVT neurons are activated by contexts/cues associated with reward (Choi et al, 2010; Igelstrom et al, 2010; Li et al, 2016; Matzeu et al, 2015; Schiltz et al, 2007) or aversion (Beck and Fibiger, 1995; Do-Monte et al, 2015b; Penzo et al, 2015; Yasoshima et al, 2007; Zhu et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Thalamic Regulation of Sucrose Seeking during Unexpected Reward Omission

Monte

Minier-Toribio

Quiñones-Laracuente

et al. 2017

Neuron

152

197

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SUMMARY The paraventricular nucleus of the thalamus (PVT) is thought to regulate behavioral responses under emotionally arousing conditions. Reward-associated cues activate PVT neurons, however, the specific PVT efferents regulating reward-seeking remain elusive. Using a cued sucrose-seeking task, we manipulated PVT activity under two emotionally distinct conditions: 1) when reward was available during the cue as expected, or 2) when reward was unexpectedly omitted during the cue. Pharmacological inactivation of the anterior PVT (aPVT), but not the posterior PVT, increased sucrose-seeking only when reward was omitted. Consistent with this, photoactivation of aPVT neurons abolished sucrose-seeking, and the firing of aPVT neurons differentiated reward availability. Photoinhibition of aPVT projections to the nucleus accumbens or to the amygdala increased or decreased, respectively, sucrose-seeking only when reward was omitted. Our findings suggest that PVT bidirectionally modulates sucrose-seeking under the negative (frustrative) conditions of reward omission.

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Amygdalo-striatal interaction in the enhancement of stimulus salience in associative learning.

Cited by 10 publications

References 44 publications

Mini-review: Prediction errors, attention and associative learning

Mini-review: Prediction errors, attention and associative learning

Dorsolateral striatum is critical for the expression of surprise‐induced enhancements in cue associability

Thalamic Regulation of Sucrose Seeking during Unexpected Reward Omission

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