Neural substrates of appetitive and aversive prediction error

Iordanova, Mihaela D.; Yau, Joanna Oi-Yue; McDannald, Michael A.; Corbit, Laura H.

doi:10.1016/j.neubiorev.2020.10.029

Cited by 45 publications

(29 citation statements)

References 198 publications

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“…Extinction procedures engage multiple neural circuits that mediate not only the retrieval and expression of conditioned responses, but also the encoding of prediction errors and contextual stimuli associated with the extinction contingency ( Bouton et al, 2006 , 2021 ; Radulovic and Tronson, 2010 ; Maren et al, 2013 ). Brainstem circuits are critical for encoding prediction errors that drive extinction learning and they convey this information to forebrain circuits that encode context-dependent extinction memories ( McNally et al, 2011 ; Iordanova et al, 2021 ). A critical hub for extinction learning is centered in the medial prefrontal cortex (mPFC) and its connections with the hippocampus (HPC) and amygdala ( Maren and Quirk, 2004 ; Quirk and Mueller, 2008 ; Orsini and Maren, 2012 ; Maren et al, 2013 ; Giustino and Maren, 2015 ; Bouton et al, 2021 ).…”

Section: Stress Modulates Neural Circuits Critical For Extinction Lea...mentioning

confidence: 99%

Unrelenting Fear Under Stress: Neural Circuits and Mechanisms for the Immediate Extinction Deficit

Maren

2022

Front. Syst. Neurosci.

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Therapeutic interventions for disorders of fear and anxiety rely on behavioral approaches that reduce pathological fear memories. For example, learning that threat-predictive stimuli are no longer associated with aversive outcomes is central to the extinction of conditioned fear responses. Unfortunately, fear memories are durable, long-lasting, and resistant to extinction, particularly under high levels of stress. This is illustrated by the “immediate extinction deficit,” which is characterized by a poor long-term reduction of conditioned fear when extinction procedures are attempted within hours of fear conditioning. Here, I will review recent work that has provided new insight into the neural mechanisms underlying resistance to fear extinction. Emerging studies reveal that locus coeruleus norepinephrine modulates amygdala-prefrontal cortical circuits that are critical for extinction learning. These data suggest that stress-induced activation of brain neuromodulatory systems biases fear memory at the expense of extinction learning. Behavioral and pharmacological strategies to reduce stress in patients undergoing exposure therapy might improve therapeutic outcomes.

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Section: Stress Modulates Neural Circuits Critical For Extinction Lea...mentioning

confidence: 99%

Unrelenting Fear Under Stress: Neural Circuits and Mechanisms for the Immediate Extinction Deficit

Maren

2022

Front. Syst. Neurosci.

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“…The ventral tegmental area (VTA), in particular its dopamine neurons, is widely implicated in reward prediction error encoding (Bromberg-Martin et al, 2010;Iordanova et al, 2021;Schultz, 1998Schultz, , 2016 and has recently shown to be important for both fear learning and fear extinction (Kalisch et al, 2019). VTA dopamine neurons are excited by an unexpected shock omission (Cai et al, 2020;de Jong et al, 2019;Salinas-Hernández et al, 2018) and this excitation is necessary for fear extinction learning because inhibiting VTA TH neurons at the time of shock omission impairs extinction (Cai et al, 2020;Luo et al, 2018;Salinas-Hernández et al, 2018).…”

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confidence: 99%

The activity of ventral tegmental area dopamine neurons during shock omission predicts safety learning.

Yau¹,

McNally²

2022

Behavioral Neuroscience

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We studied the role of dopamine [tyrosine hydroxylase (TH)] neurons in the rat ventral tegmental area (VTA) in safety learning. First, we used an AX+/BX-discrimination procedure to establish conditioned stimulus (CS) B as a learned safety signal that passed both summation and retardation tests of conditioned inhibition. Then, we combined this procedure with fiber photometry in TH-Cre rats to study the activity of VTA dopamine neurons during safety learning. We show that whereas footshock is associated with calcium transients in TH neurons across the VTA, shock omission during safety learning is selectively associated with calcium transients in dopamine neurons in the medial but not lateral VTA. Moreover, the magnitude of medial VTA calcium transients during shock omission accurately predicts the amount of safety that is learned and expressed during summation testing. Our findings are consistent with a common medial VTA dopamine mechanism contributing to the learned inhibition of fear in extinction and safety.

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“…Studies in fear suggest that one potential mediator of BLA-CN interaction is the locus coeruleus (LC; Cedarbaum and Aghajanian, 1978; Giustino and Maren, 2018; Valentino and Van Bockstaele, 2008; Van Bockstaele et al, 1998). Neuropeptide corticotropin-releasing factor (CRF) expressing neurons in the CN promote the activity of noradrenergic neurons in the LC that project to BLA (McCall et al, 2015; see also Prouty et al, 2017; Schwarz et al, 2015; Van Bockstaele et al ., 1998 see Iordanova, Yau, McDannald, & Corbit, 2021 for review of LC in extinction), rendering conditioned responding (in fear) more persistent in general (Giustino et al, 2020; Sanford et al, 2017; see also Uematsu et al, 2017) and in the face of extinction (Abiri et al, 2014; Giustino et al ., 2020; Sanford et al ., 2017; see also Uematsu et al ., 2017). Therefore, it is possible that extinction might hinder the ability of CRF-neurons in CN to boost the activity of BLA acquisition ensembles (via LC activation, Giustino and Maren, 2018), limiting the latter’s influence over behaviour.…”

Section: Discussionmentioning

confidence: 99%

A critical contribution of a sparse neuronal ensemble in the amygdala central nucleus to extinction

Lay

Koya

Hope

et al. 2022

Preprint

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Adaptive behaviour critically depends on the delicate and dynamic balance between acquisition and extinction memories. Disruption of this balance, particularly when the extinction memory loses control over behaviour, is the root of treatment failure of maladaptive behaviours such as substance abuse or anxiety disorders. Understanding this balance requires a better understanding of the underlying neurobiology and its contribution to behavioural regulation. Here, we used Daun02 in Fos-lacZ transgenic rats to delete extinction-recruited neuronal ensembles in BLA and CN and examine their contribution to behaviour in an appetitive Pavlovian task. Deletion of extinction-activated ensembles in CN but not BLA impaired the retrieval of extinction and increased activity in the BLA. The disruptive effect of deleting these CN ensembles was enduring as it hindered further extinction learning, and promoted greater levels of behavioural restoration across opposing levels of the response scale seen in spontaneous recovery and reinstatement. Our data indicate that the initial extinction-recruited CN ensemble is critical to the acquisition-extinction balance, and that greater behavioural restoration does not mean weaker extinction contribution. These findings provide a novel avenue for thinking about the neural mechanisms of extinction and in developing treatments for cue-triggered appetitive behaviours.

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Neural substrates of appetitive and aversive prediction error

Cited by 45 publications

References 198 publications

Unrelenting Fear Under Stress: Neural Circuits and Mechanisms for the Immediate Extinction Deficit

Unrelenting Fear Under Stress: Neural Circuits and Mechanisms for the Immediate Extinction Deficit

The activity of ventral tegmental area dopamine neurons during shock omission predicts safety learning.

A critical contribution of a sparse neuronal ensemble in the amygdala central nucleus to extinction

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