Synergy of Distinct Dopamine Projection Populations in Behavioral Reinforcement

Heymann, Gabriel; Jo, Yong Sang; Reichard, Kathryn L.; McFarland, Naomi; Chavkin, Charles; Palmiter, Richard D.; Soden, Marta E.; Zweifel, Larry S.

doi:10.1016/j.neuron.2019.11.024

Cited by 115 publications

(128 citation statements)

References 56 publications

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“…It is well established that there are heterogenous response profiles across the mesolimbic dopamine system that serve distinct functions (Cohen et al, 2012;de Jong et al, 2019;Heymann et al, 2019;Lammel et al, 2008;Lammel et al, 2011;Lammel et al, 2013;Mohebi et al, 2019;Saunders et al, 2018;Tian et al, 2016;Watabe-Uchida et al, 2012). Our findings support this.…”

Section: Discussionsupporting

confidence: 86%

“…However, the mesolimbic dopamine system has a complex architecture. VTA dopamine neurons form distinct channels linked to differences in behavioral and motivational function (Cohen et al, 2012;de Jong et al, 2019;Heymann et al, 2019;Lammel et al, 2008;Lammel et al, 2011;Lammel et al, 2013;Saunders et al, 2018;Tian et al, 2016;Watabe-Uchida et al, 2012). In turn, there are distinct profiles of dopamine release across compartments of the ventral striatum giving rise to different functions (de Jong et al, 2019;Mohebi et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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The mesolimbic dopamine signatures of relapse to alcohol-seeking

Liu

Bressel

Yau

et al. 2020

Preprint

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The mesolimbic dopamine system comprises distinct compartments supporting different functions in learning and motivation. Less well understood is how complex addiction-related behaviors emerge from activity patterns across these compartments. Here we show how different forms of relapse to alcohol-seeking are assembled from activity across the ventral tegmental area and the nucleus accumbens. Using gCaMP and dLight fibre photometry, we show that self-administration and two forms of relapse (renewal/context-induced reinstatement and reacquisition) are associated with recruitment across the mesolimbic dopamine system. Using a variety of interventions, we show that this activity is causal to both forms of relapse. Finally, we use dissimilarity matrices to identify mesolimbic dopamine signatures of self-administration, extinction, and relapse. We show that signatures of relapse can be identified from heterogeneous activity profiles across the mesolimbic dopamine system and that these signatures differ for different forms of relapse.

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Section: Discussionsupporting

confidence: 86%

Section: Introductionmentioning

confidence: 99%

The mesolimbic dopamine signatures of relapse to alcohol-seeking

Liu

Bressel

Yau

et al. 2020

Preprint

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“…We and others have previously demonstrated considerable functional diversity among SNc/VTA dopamine neurons (de Jong et al, 2019;Evans et al, 2017;Heymann et al, 2020;Lammel et al, 2008;Tarfa et al, 2017). This diversity was in part associated with distinct axonal projections both in vitro (Lammel et al, 2008) and in vivo (Farassat et al, 2019).…”

Section: Resultsmentioning

confidence: 84%

“…For many years, transient cue-or reward-associated increases in firing rate -from a low tonic background frequency (about 1-8 Hz) into the beta and gamma range (15-30 Hz and 40-100 Hz, respectively) -were thought to encode positive reward prediction errors (RPEs), while short rate reductions or pauses in baseline firing were believed to encode negative RPEs, induced for instance by the omission of an expected reward. However, increasing experimental evidence points to a multitude of other dopamine functions such as salience and novelty, action control (Coddington and Dudman, 2018;Jin and Costa, 2010) as well as aversion (Menegas et al, 2018) which are in line with the emerging molecular (Heymann et al, 2020;Poulin et al, 2020), cellular, and anatomical diversity of the midbrain dopamine system (Beier et al, 2019;Beier et al, 2015;Farassat et al, 2019;Lammel et al, 2008;Lammel et al, 2012;Morales and Margolis, 2017;Watabe-Uchida et al, 2012). Even within canonical RPE signaling, the interpretation of the transient burst has become more complex.…”

Section: Mainmentioning

confidence: 99%

Subthreshold repertoire and threshold dynamics of midbrain dopamine neuron firingin vivo

Otomo

Perkins

Kulkarni

et al. 2020

Preprint

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The firing pattern of ventral midbrain dopamine neurons is controlled by afferent and intrinsic activity to generate prediction error signals that are essential for reward-based learning. Given the absence of intracellular in vivo recordings in the last three decades, the subthreshold membrane potential events that cause changes in dopamine neuron firing patterns remain unknown. By establishing stable in vivo whole-cell recordings of >100 spontaneously active midbrain dopamine neurons in anaesthetized mice, we identified the repertoire of subthreshold membrane potential signatures associated with distinct in vivo firing patterns. We demonstrate that in vivo activity of dopamine neurons deviates from a single spike pacemaker pattern by eliciting transient increases in firing rate generated by at least two diametrically opposing biophysical mechanisms: a transient depolarization resulting in high frequency plateau bursts associated with a reactive depolarizing shift in action potential threshold, and a prolonged hyperpolarization preceding slower rebound bursts characterized by a predictive hyperpolarizing shift in action potential threshold. Our findings therefore illustrate a framework for the biophysical implementation of prediction error coding in dopamine neurons by tuning action potential threshold dynamics.

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“…Dopamine neurons projecting to the striatum are genetically and functionally diverse [25][26][27]. While rewards and reward-predictive cues elicit dopamine release in the NAc core and medial NAc shell, regional differences in the dynamics of the dopamine response are evident in some tasks [11][12][13]22,23].…”

Section: Discussionmentioning

confidence: 99%

Dopamine release and its control over early Pavlovian learning differs between the NAc core and medial NAc shell

Stelly

Girven

Lefner

et al. 2020

Preprint

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Dopamine neurons respond to cues to reflect the value of associated outcomes. These cue-evoked dopamine responses can encode the relative rate of reward in rats with extensive Pavlovian training. Specifically, a cue that always follows the previous reward by a short delay (high reward rate) evokes a larger dopamine response in the nucleus accumbens (NAc) core relative to a distinct cue that always follows the prior reward by a long delay (low reward rate). However, it was unclear if these reward rate dopamine signals are evident during early Pavlovian training sessions and across NAc subregions. To address this, we performed fast-scan cyclic voltammetry recordings of dopamine levels to track the pattern of cue and reward-evoked dopamine signals in the NAc core and medial NAc shell. We identified regional differences in the progression of cue-evoked dopamine signals. However, reward rate encoding was not evident in either the NAc core or NAc shell during early training sessions. Pharmacological experiments found that dopamine-sensitive conditioned responding emerged in the NAc core before the NAc shell. Together, these findings illustrate regional differences in NAc dopamine release and its control over behavior during early Pavlovian learning.

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Synergy of Distinct Dopamine Projection Populations in Behavioral Reinforcement

Cited by 115 publications

References 56 publications

The mesolimbic dopamine signatures of relapse to alcohol-seeking

The mesolimbic dopamine signatures of relapse to alcohol-seeking

Subthreshold repertoire and threshold dynamics of midbrain dopamine neuron firingin vivo

Dopamine release and its control over early Pavlovian learning differs between the NAc core and medial NAc shell

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