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Article ; Online: Special issue on conditioned determinants of reward seeking: a tribute to Dr. Nadia Chaudhri.

Janak, Patricia H / Shaham, Yavin

2023 Volume 240, Issue 3, Page(s) 391–392

Language	English
Publishing date	2023-02-01
Publishing country	Germany
Document type	Editorial
ZDB-ID	130601-7
ISSN	1432-2072 ; 0033-3158
ISSN (online)	1432-2072
ISSN	0033-3158
DOI	10.1007/s00213-023-06326-6
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Article ; Online: Basolateral amygdala and orbitofrontal cortex, but not dorsal hippocampus, are necessary for the control of reward-seeking by occasion setters.

Fraser, Kurt M / Janak, Patricia H

Psychopharmacology

2022 Volume 240, Issue 3, Page(s) 623–635

Abstract: Reward-seeking in the world is driven by cues that can have ambiguous predictive and motivational value. To produce adaptive, flexible reward-seeking, it is necessary to exploit occasion setters, other distinct features in the environment, to resolve the ...

Abstract	Reward-seeking in the world is driven by cues that can have ambiguous predictive and motivational value. To produce adaptive, flexible reward-seeking, it is necessary to exploit occasion setters, other distinct features in the environment, to resolve the ambiguity of Pavlovian reward-paired cues. Despite this, very little research has investigated the neurobiological underpinnings of occasion setting, and as a result little is known about which brain regions are critical for occasion setting. To address this, we exploited a recently developed task that was amenable to neurobiological inquiry where a conditioned stimulus is only predictive of reward delivery if preceded in time by the non-overlapping presentation of a separate cue-an occasion setter. This task required male rats to maintain and link cue-triggered expectations across time to produce adaptive reward-seeking. We interrogated the contributions of the basolateral amygdala and orbitofrontal cortex to occasion setting as these regions are thought to be critical for the computation and exploitation of state value, respectively. Reversible inactivation of either structure prior to the occasion-setting task resulted in a profound inability of rats to use the occasion setter to guide reward-seeking. In contrast, inactivation of the dorsal hippocampus, a region fundamental for context-specific responding was without effect nor did inactivation of the basolateral amygdala or orbitofrontal cortex in a standard Pavlovian conditioning preparation affect conditioned responding. We conclude that neural activity within the orbitofrontal cortex and basolateral amygdala circuit is necessary to update and resolve ambiguity in the environment to promote cue-driven reward-seeking.
MeSH term(s)	Rats ; Male ; Animals ; Basolateral Nuclear Complex/physiology ; Reward ; Prefrontal Cortex/physiology ; Conditioning, Operant ; Cues ; Hippocampus/physiology
Language	English
Publishing date	2022-09-03
Publishing country	Germany
Document type	Journal Article
ZDB-ID	130601-7
ISSN	1432-2072 ; 0033-3158
ISSN (online)	1432-2072
ISSN	0033-3158
DOI	10.1007/s00213-022-06227-0
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Article ; Online: Nucleus accumbens and dorsal medial striatal dopamine and neural activity are essential for action sequence performance.

Fraser, Kurt M / Chen, Bridget J / Janak, Patricia H

The European journal of neuroscience

2023 Volume 59, Issue 2, Page(s) 220–237

Abstract: Separable striatal circuits have unique functions in Pavlovian and instrumental behaviors but how these roles relate to performance of sequences of actions with and without associated cues are less clear. Here, we tested whether dopamine transmission and ...

Abstract	Separable striatal circuits have unique functions in Pavlovian and instrumental behaviors but how these roles relate to performance of sequences of actions with and without associated cues are less clear. Here, we tested whether dopamine transmission and neural activity more generally in three striatal subdomains are necessary for performance of an action chain leading to reward delivery. Male and female Long-Evans rats were trained to press a series of three spatially distinct levers to receive reward. We assessed the contribution of neural activity or dopamine transmission within each striatal subdomain when progression through the action sequence was explicitly cued and in the absence of cues. Behavior in both task variations was substantially impacted following microinfusion of the dopamine antagonist, flupenthixol, into nucleus accumbens core (NAc) or dorsomedial striatum (DMS), with impairments in sequence timing and numbers of rewards earned after NAc flupenthixol. In contrast, after pharmacological inactivation to suppress overall activity, there was minimal impact on total rewards earned. Instead, inactivation of both NAc and DMS impaired sequence timing and led to sequence errors in the uncued, but not cued task. There was no impact of dopamine antagonism or reversible inactivation of dorsolateral striatum on either cued or uncued action sequence completion. These results highlight an essential contribution of NAc and DMS dopamine systems in motivational and performance aspects of chains of actions, whether cued or internally generated, as well as the impact of intact NAc and DMS function for correct sequence performance.
MeSH term(s)	Female ; Rats ; Animals ; Male ; Rats, Long-Evans ; Nucleus Accumbens ; Dopamine ; Flupenthixol/pharmacology ; Motivation ; Cues ; Dopamine Antagonists/pharmacology ; Reward ; Conditioning, Operant
Chemical Substances	Dopamine (VTD58H1Z2X) ; Flupenthixol (FA0UYH6QUO) ; Dopamine Antagonists
Language	English
Publishing date	2023-12-13
Publishing country	France
Document type	Journal Article
ZDB-ID	645180-9
ISSN	1460-9568 ; 0953-816X
ISSN (online)	1460-9568
ISSN	0953-816X
DOI	10.1111/ejn.16210
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Article ; Online: Consolidating the Circuit Model for Addiction.

Lüscher, Christian / Janak, Patricia H

Annual review of neuroscience

2021 Volume 44, Page(s) 173–195

Abstract: Addiction is a disease characterized by compulsive drug seeking and consumption observed in 20-30% of users. An addicted individual will favor drug reward over natural rewards, despite major negative consequences. Mechanistic research on rodents modeling ...

Abstract	Addiction is a disease characterized by compulsive drug seeking and consumption observed in 20-30% of users. An addicted individual will favor drug reward over natural rewards, despite major negative consequences. Mechanistic research on rodents modeling core components of the disease has identified altered synaptic transmission as the functional substrate of pathological behavior. While the initial version of a circuit model for addiction focused on early drug adaptive behaviors observed in all individuals, it fell short of accounting for the stochastic nature of the transition to compulsion. The model builds on the initial pharmacological effect common to all addictive drugs-an increase in dopamine levels in the mesolimbic system. Here, we consolidate this early model by integrating circuits underlying compulsion and negative reinforcement. We discuss the genetic and epigenetic correlates of individual vulnerability. Many recent data converge on a gain-of-function explanation for circuit remodeling, revealing blueprints for novel addiction therapies.
MeSH term(s)	Behavior, Addictive ; Drug-Seeking Behavior ; Humans ; Reinforcement, Psychology ; Reward ; Substance-Related Disorders
Language	English
Publishing date	2021-03-05
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	282459-0
ISSN	1545-4126 ; 0147-006X
ISSN (online)	1545-4126
ISSN	0147-006X
DOI	10.1146/annurev-neuro-092920-123905
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Article: Basolateral amygdala population coding of a cued reward seeking state depends on orbitofrontal cortex.

Ottenheimer, David J / Vitale, Katherine R / Ambroggi, Frederic / Janak, Patricia H / Saunders, Benjamin T

bioRxiv : the preprint server for biology

2024

Abstract: Basolateral amygdala (BLA) neuronal responses to conditioned stimuli are closely linked to the expression of conditioned behavior. An area of increasing interest is how the dynamics of BLA neurons relate to evolving behavior. Here, we recorded the ... ...

Abstract	Basolateral amygdala (BLA) neuronal responses to conditioned stimuli are closely linked to the expression of conditioned behavior. An area of increasing interest is how the dynamics of BLA neurons relate to evolving behavior. Here, we recorded the activity of individual BLA neurons across the acquisition and extinction of conditioned reward seeking and employed population-level analyses to assess ongoing neural dynamics. We found that, with training, sustained cue-evoked activity emerged that discriminated between the CS+ and CS- and correlated with conditioned responding. This sustained population activity continued until reward receipt and rapidly extinguished along with conditioned behavior during extinction. To assess the contribution of orbitofrontal cortex (OFC), a major reciprocal partner to BLA, to this component of BLA neural activity, we inactivated OFC while recording in BLA and found blunted sustained cue-evoked activity in BLA that accompanied reduced reward seeking. Optogenetic disruption of BLA activity and OFC terminals in BLA also reduced reward seeking. Our data suggest that sustained cue-driven activity in BLA, which in part depends on OFC input, underlies conditioned reward-seeking states.
Language	English
Publishing date	2024-01-01
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.12.31.573789
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Article: Pavlovian cue-evoked alcohol seeking is disrupted by ventral pallidal inhibition.

Richard, Jocelyn M / Armstrong, Anne / Newell, Bailey / Muruganandan, Preethi / Janak, Patricia H / Saunders, Benjamin T

bioRxiv : the preprint server for biology

2024

Abstract: Cues paired with alcohol can be potent drivers of craving, alcohol-seeking, consumption, and relapse. While the ventral pallidum is implicated in appetitive and consummatory responses across several reward classes and types of behaviors, its role in ... ...

Abstract	Cues paired with alcohol can be potent drivers of craving, alcohol-seeking, consumption, and relapse. While the ventral pallidum is implicated in appetitive and consummatory responses across several reward classes and types of behaviors, its role in behavioral responses to Pavlovian alcohol cues has not previously been established. Here, we tested the impact of optogenetic inhibition of ventral pallidum on Pavlovian-conditioned alcohol-seeking in male Long Evans rats. Rats underwent Pavlovian conditioning with an auditory cue predicting alcohol delivery to a reward port and a control cue predicting no alcohol delivery, until they consistently entered the reward port more during the alcohol cue than the control cue. We then tested the within-session effects of optogenetic inhibition during 50% of cue presentations. We found that optogenetic inhibition of ventral pallidum during the alcohol cue reduced port entry likelihood and time spent in the port, and increased port entry latency. Overall, these results suggest that normal ventral pallidum activity is necessary for Pavlovian alcohol-seeking.
Language	English
Publishing date	2024-03-14
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.03.14.585064
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Article: Chronic Ethanol Exposure Produces Persistent Impairment in Cognitive Flexibility and Decision Signals in the Striatum.

Cheng, Yifeng / Magnard, Robin / Langdon, Angela J / Lee, Daeyeol / Janak, Patricia H

bioRxiv : the preprint server for biology

2024

Abstract: Lack of cognitive flexibility is a hallmark of substance use disorders and has been associated with drug-induced synaptic plasticity in the dorsomedial striatum (DMS). Yet the possible impact of altered plasticity on real-time striatal neural dynamics ... ...

Abstract	Lack of cognitive flexibility is a hallmark of substance use disorders and has been associated with drug-induced synaptic plasticity in the dorsomedial striatum (DMS). Yet the possible impact of altered plasticity on real-time striatal neural dynamics during decision-making is unclear. Here, we identified persistent impairments induced by chronic ethanol (EtOH) exposure on cognitive flexibility and striatal decision signals. After a substantial withdrawal period from prior EtOH vapor exposure, male, but not female, rats exhibited reduced adaptability and exploratory behavior during a dynamic decision-making task. Reinforcement learning models showed that prior EtOH exposure enhanced learning from rewards over omissions. Notably, neural signals in the DMS related to the decision outcome were enhanced, while those related to choice and choice-outcome conjunction were reduced, in EtOH-treated rats compared to the controls. These findings highlight the profound impact of chronic EtOH exposure on adaptive decision-making, pinpointing specific changes in striatal representations of actions and outcomes as underlying mechanisms for cognitive deficits.
Language	English
Publishing date	2024-03-29
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.03.10.584332
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Article ; Online: From Prediction to Action: Dissociable Roles of Ventral Tegmental Area and Substantia Nigra Dopamine Neurons in Instrumental Reinforcement.

Fraser, Kurt M / Pribut, Heather J / Janak, Patricia H / Keiflin, Ronald

The Journal of neuroscience : the official journal of the Society for Neuroscience

2023 Volume 43, Issue 21, Page(s) 3895–3908

Abstract: Reward seeking requires the coordination of motor programs to achieve goals. Midbrain dopamine neurons are critical for reinforcement, and their activation is sufficient for learning about cues, actions, and outcomes. Here we examine in detail the ... ...

Abstract	Reward seeking requires the coordination of motor programs to achieve goals. Midbrain dopamine neurons are critical for reinforcement, and their activation is sufficient for learning about cues, actions, and outcomes. Here we examine in detail the mechanisms underlying the ability of ventral tegmental area (VTA) and substantia nigra (SNc) dopamine neurons to support instrumental learning. By exploiting numerous behavioral tasks in combination with time-limited optogenetic manipulations in male and female rats, we reveal that VTA and SNc dopamine neurons generate reinforcement through separable psychological processes. VTA dopamine neurons imbue actions and their associated cues with motivational value that allows flexible and persistent pursuit, whereas SNc dopamine neurons support time-limited, precise, action-specific learning that is nonscalable and inflexible. This architecture is reminiscent of actor-critic reinforcement learning models with VTA and SNc instructing the critic and actor, respectively. Our findings indicate that heterogeneous dopamine systems support unique forms of instrumental learning that ultimately result in disparate reward-seeking strategies.
MeSH term(s)	Rats ; Male ; Female ; Animals ; Dopaminergic Neurons/physiology ; Ventral Tegmental Area/physiology ; Reinforcement, Psychology ; Substantia Nigra/physiology ; Reward
Language	English
Publishing date	2023-04-25
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	604637-x
ISSN	1529-2401 ; 0270-6474
ISSN (online)	1529-2401
ISSN	0270-6474
DOI	10.1523/JNEUROSCI.0028-23.2023
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Article ; Online: Decreases in Cued Reward Seeking After Reward-Paired Inhibition of Mesolimbic Dopamine.

Fischbach, Sarah / Janak, Patricia H

Neuroscience

2019 Volume 412, Page(s) 259–269

Abstract: Reward-paired optogenetic manipulation of dopamine neurons can increase or decrease behavioral responding to antecedent cues when subjects have the opportunity for new learning, in accordance with a dopamine-mediated error learning signal. Here we ... ...

Abstract	Reward-paired optogenetic manipulation of dopamine neurons can increase or decrease behavioral responding to antecedent cues when subjects have the opportunity for new learning, in accordance with a dopamine-mediated error learning signal. Here we examined the impact of reward-paired dopamine neuron inhibition on behavioral responding to reward-predictive cues after subjects had learned. We trained male TH-IRES-Cre mice to lever press for food reward in a progressive ratio procedure, a 2-cue choice procedure, or when continuously reinforced; in all procedures, completion of the response requirement was signaled by an auditory cue presented prior to food delivery. After training, mice underwent successive sessions in which optogenetic inhibition of dopamine neurons was triggered during food receipt. Rather than mimic brief inhibitions associated with negative reward prediction errors, we applied inhibition throughout the ingestion period on each trial. We found in all procedures that optogenetic inhibition of dopamine neurons during reward receipt decreased behavioral responding to the preceding reward-predictive cue over days, a behavioral change observed during time periods without optogenetic neuronal inhibition. Extinction-like behavioral responding was selective for learned associations: it was observed in the 2-cue choice procedure in which each subject was trained on two associations and inhibition was paired with reward for only one of the associations. Thus, inhibition during reward receipt can decrease responding to reward-predictive cues, sharing some features of behavioral extinction. These findings suggest changes in mesolimbic dopaminergic transmission at the time of experienced reward impacts subsequent responding to cues in well-trained subjects as predicted for a learning signal.
MeSH term(s)	Acoustic Stimulation ; Animals ; Association Learning/physiology ; Conditioning, Operant/physiology ; Cues ; Dopaminergic Neurons/physiology ; Male ; Mice ; Motivation/physiology ; Optogenetics ; Reward ; Ventral Tegmental Area/physiology
Language	English
Publishing date	2019-04-25
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	196739-3
ISSN	1873-7544 ; 0306-4522
ISSN (online)	1873-7544
ISSN	0306-4522
DOI	10.1016/j.neuroscience.2019.04.035
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Article ; Online: Dorsomedial Striatal Activity Tracks Completion of Behavioral Sequences in Rats.

Vandaele, Youna / Ottenheimer, David J / Janak, Patricia H

eNeuro

2021 Volume 8, Issue 6

Abstract: For proper execution of goal-directed behaviors, individuals require both a general representation of the goal and an ability to monitor their own progress toward that goal. Here, we examine how dorsomedial striatum (DMS), a region pivotal for forming ... ...

Abstract	For proper execution of goal-directed behaviors, individuals require both a general representation of the goal and an ability to monitor their own progress toward that goal. Here, we examine how dorsomedial striatum (DMS), a region pivotal for forming associations among stimuli, actions, and outcomes, encodes the execution of goal-directed action sequences that require self-monitoring of behavior. We trained rats to complete a sequence of at least five consecutive lever presses (without visiting the reward port) to obtain a reward and recorded the activity of individual cells in DMS while rats performed the task. We found that the pattern of DMS activity gradually changed during the execution of the sequence, permitting accurate decoding of sequence progress from neural activity at a population level. Moreover, this sequence-related activity was blunted on trials where rats did not complete a sufficient number of presses. Overall, these data suggest a link between DMS activity and the execution of behavioral sequences that require monitoring of ongoing behavior.
MeSH term(s)	Animals ; Corpus Striatum ; Humans ; Motivation ; Neostriatum ; Rats ; Reward
Language	English
Publishing date	2021-11-18
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2800598-3
ISSN	2373-2822 ; 2373-2822
ISSN (online)	2373-2822
ISSN	2373-2822
DOI	10.1523/ENEURO.0279-21.2021
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