Fos Activation of Selective Afferents to Ventral Tegmental Area during Cue-Induced Reinstatement of Cocaine Seeking in Rats

Ventral tegmental area (VTA) dopamine neurons are crucial for appetitive responses to Pavlovian cues, including cue-induced reinstatement of drug seeking. However, it is unknown which VTA inputs help activate these neurons, transducing stimuli into salient cues that drive drug-seeking behavior. Here we examined 56 VTA afferents from forebrain and midbrain that are Fos activated during cue-induced reinstatement. We injected the retrograde tracer cholera toxin β subunit (CTb) unilaterally into rostral or caudal VTA of male rats. All animals were trained to self-administer cocaine, then extinguished of this behavior. On a final test day, animals were exposed to response-contingent cocaine-associated cues, extinction conditions, a non-cocaine-predictive CS−, or a novel environment, and brains were processed to visualize CTb and Fos immunoreactivity to identify VTA afferents activated in relation to behaviors. VTA-projecting neurons in subregions of medial accumbens shell, ventral pallidum, elements of extended amygdala, and lateral septum (but not prefrontal cortex) were activated specifically during cue-induced cocaine seeking, and some of these were also activated proportionately to the degree of cocaine seeking. Surprisingly, though efferents from the lateral hypothalamic orexin field were also Fos activated during reinstatement, these were largely non-orexinergic. Also, VTA afferents from the rostromedial tegmental nucleus and lateral habenula were specifically activated during extinction and CS− tests, when cocaine was not expected. These findings point to a select set of subcortical nuclei which provide reinstatement-related inputs to VTA, translating conditioned stimuli into cocaine-seeking behavior.

• Publication year

  2012

• Venue

  Journal of Neuroscience

• Publication date

  2012-09-19

• Fields of study

  Biology, Medicine, Psychology

• Identifiers
  DOI 10.1523/JNEUROSCI.2277-12.2012PMID 22993446PMCID PMC3480730
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• On lateral septum‐like characteristics of outputs from the accumbal hedonic “hotspot” of Peciña and Berridge with commentary on the transitional nature of basal forebrain “boundaries”

  2013influential reference
• Multiple roles for orexin/hypocretin in addiction.

  2012influential reference
• Interactions between VTA orexin and glutamate in cue-induced reinstatement of cocaine seeking in rats

  2012influential reference
• Orexin ⁄ hypocretin 1 receptor antagonist reduces heroin self-administration and cue-induced heroin seeking

  2012influential reference
• Orexin / hypocretin 1 receptor antagonist reduces heroin self‐administration and cue‐induced heroin seeking

  2012cited by this paper
• Lateral Hypothalamic Orexin/Hypocretin Neurons That Project to Ventral Tegmental Area Are Differentially Activated with Morphine Preference

  2012cited by this paper
• A Septal-Hypothalamic Pathway Drives Orexin Neurons, Which Is Necessary for Conditioned Cocaine Preference

  2012influential reference
• Differential projections from the lateral habenula to the rostromedial tegmental nucleus and ventral tegmental area in the rat

  2012cited by this paper
• Orexinergic innervation of the extended amygdala and basal ganglia in the rat

  2012cited by this paper
• Nucleus Accumbens Dopamine/Glutamate Interaction Switches Modes to Generate Desire versus Dread: D1 Alone for Appetitive Eating But D1 and D2 Together for Fear

  2011cited by this paper
• Sensitized activation of Fos and brain-derived neurotrophic factor in the medial prefrontal cortex and ventral tegmental area accompanies behavioral sensitization to amphetamine.

  2011cited by this paper
• Disentangling pleasure from incentive salience and learning signals in brain reward circuitry

  2011cited by this paper
• Heterogeneous processing of amygdala and hippocampal inputs in the rostral and caudal subregions of the nucleus accumbens.

  2011cited by this paper
• Glutamate and GABA in lateral hypothalamic mechanisms controlling food intake.

  2011cited by this paper
• Common biology of craving across legal and illegal drugs – a quantitative meta‐analysis of cue‐reactivity brain response

  2011cited by this paper
• Orexin-1 receptor signalling within the ventral tegmental area, but not the paraventricular thalamus, is critical to regulating cue-induced reinstatement of cocaine-seeking.

  2011influential reference
• Linking Context with Reward: A Functional Circuit from Hippocampal CA3 to Ventral Tegmental Area

  2011influential reference
• The inhibitory influence of the lateral habenula on midbrain dopamine cells: Ultrastructural evidence for indirect mediation via the rostromedial mesopontine tegmental nucleus

  2011cited by this paper
• Negative Reward Signals from the Lateral Habenula to Dopamine Neurons Are Mediated by Rostromedial Tegmental Nucleus in Primates

  2011cited by this paper
• Nucleus Accumbens Medium Spiny Neurons Target Non-Dopaminergic Neurons in the Ventral Tegmental Area

  2011cited by this paper
• Inactivation of the bed nucleus of the stria terminalis in an animal model of relapse: effects on conditioned cue-induced reinstatement and its enhancement by yohimbine

  2010cited by this paper
• Cortico-Basal Ganglia Reward Network: Microcircuitry

  2010cited by this paper
• Dopamine signals for reward value and risk: basic and recent data

  2010cited by this paper
• Hypothesis-driven structural connectivity analysis supports network over hierarchical model of brain architecture

  2010influential reference
• Ventral Tegmental Afferents in Stress-Induced Reinstatement: The Role of cAMP Response Element-Binding Protein

  2010cited by this paper
• Orexin/hypocretin is necessary for context-driven cocaine-seeking.

  2010cited by this paper
• gamma-Aminobutyric acid cells with cocaine-induced DeltaFosB in the ventral tegmental area innervate mesolimbic neurons.

  2010cited by this paper
• A ventral tegmental CRF-glutamate-dopamine interaction in addiction.

  2010cited by this paper
• Glutamatergic axons from the lateral habenula mainly terminate on GABAergic neurons of the ventral midbrain.

  2010cited by this paper
• Orexin/Hypocretin Modulates Response of Ventral Tegmental Dopamine Neurons to Prefrontal Activation: Diurnal Influences

  2010cited by this paper
• Mu opioid receptor knockdown in the substantia nigra/ventral tegmental area by synthetic small interfering RNA blocks the rewarding and locomotor effects of heroin.

  2009cited by this paper
• Orexin/hypocretin signaling at the orexin 1 receptor regulates cue‐elicited cocaine‐seeking

  2009influential reference
• c‐Fos expression associated with reinstatement of cocaine‐seeking behavior by response‐contingent conditioned cues

  2009cited by this paper
• The mesopontine rostromedial tegmental nucleus: A structure targeted by the lateral habenula that projects to the ventral tegmental area of Tsai and substantia nigra compacta

  2009cited by this paper
• The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses.

  2009cited by this paper
• Neuropeptide S inhibits the acquisition and the expression of conditioned place preference to morphine in mice.

  2009cited by this paper
• Effects of the MCH1 receptor antagonist SNAP 94847 on high-fat food-reinforced operant responding and reinstatement of food seeking in rats

  2009cited by this paper
• Phasic dopamine release in appetitive behaviors and drug addiction.

  2009cited by this paper
• Dynamic Computation of Incentive Salience: “Wanting” What Was Never “Liked”

  2009cited by this paper
• Adrenergic and Noradrenergic Innervation of the Midbrain Ventral Tegmental Area and Retrorubral Field: Prominent Inputs from Medullary Homeostatic Centers

  2009cited by this paper
• Lateral habenula projections to dopamine and GABA neurons in the rat ventral tegmental area

  2009influential reference
• Reinstatement of cocaine seeking by hypocretin (orexin) in the ventral tegmental area: independence from the local corticotropin-releasing factor network.

  2009cited by this paper
• The melanin-concentrating hormone system modulates cocaine reward

  2009cited by this paper
• Neurobiological substrates of cue-elicited craving and anhedonia in recently abstinent opioid-dependent males.

  2009cited by this paper
• Cocaine reward and hyperactivity in the rat: sites of mu opioid receptor modulation.

  2008cited by this paper
• Drug Addiction and the Memory Systems of the Brain

  2008cited by this paper
• Prominent Activation of Brainstem and Pallidal Afferents of the Ventral Tegmental Area by Cocaine

  2008influential reference
• Presynaptic Opioid and Nicotinic Receptor Modulation of Dopamine Overflow in the Nucleus Accumbens

  2008cited by this paper
• Prelude to Passion: Limbic Activation by “Unseen” Drug and Sexual Cues

  2008cited by this paper
• Enkephalin co‐expression with classic neurotransmitters in the amygdaloid complex of the rat

  2008cited by this paper
• A top-down perspective on dopamine, motivation and memory.

  2008cited by this paper
• Upregulation of Arc mRNA expression in the prefrontal cortex following cue‐induced reinstatement of extinguished cocaine‐seeking behavior

  2008cited by this paper
• Glutamatergic Afferents of the Ventral Tegmental Area in the Rat

  2007influential reference
• General and outcome‐specific forms of Pavlovian‐instrumental transfer: the effect of shifts in motivational state and inactivation of the ventral tegmental area

  2007cited by this paper
• Activation of afferents to the ventral tegmental area in response to acute amphetamine: a double‐labelling study

  2007influential reference
• Behavioral dopamine signals.

  2007cited by this paper
• Lateral habenula as a source of negative reward signals in dopamine neurons

  2007cited by this paper
• Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits

  2007cited by this paper
• A Role for Conditioned Ventral Tegmental Glutamate Release in Cocaine Seeking

  2007cited by this paper
• Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex.

  2007cited by this paper
• The debate over dopamine’s role in reward: the case for incentive salience

  2007cited by this paper
• Synaptologic and fine structural features distinguishing a subset of basal forebrain cholinergic neurons embedded in the dense intrinsic fiber network of the caudal extended amygdala

  2006cited by this paper
• Different effects of GABAergic receptors located in the ventral tegmental area on the expression of morphine-induced conditioned place preference in rat.

  2005cited by this paper
• Role for hypocretin in mediating stress-induced reinstatement of cocaine-seeking behavior.

  2005cited by this paper
• Hedonic Hot Spot in Nucleus Accumbens Shell: Where Do μ-Opioids Cause Increased Hedonic Impact of Sweetness?

  2005cited by this paper
• Afferents of the ventral tegmental area in the rat‐anatomical substratum for integrative functions

  2005influential reference
• A pharmacological analysis of the burst events induced in midbrain dopaminergic neurons by electrical stimulation of the prefrontal cortex in the rat

  2005cited by this paper
• A role for lateral hypothalamic orexin neurons in reward seeking

  2005influential reference
• Ethanol-induced conditioned place preference is expressed through a ventral tegmental area dependent mechanism.

  2005cited by this paper
• Cocaine-Induced Reinstatement Requires Endogenous Stimulation of μ-Opioid Receptors in the Ventral Pallidum

  2005cited by this paper
• Dopamine Operates as a Subsecond Modulator of Food Seeking

  2004cited by this paper
• Limbic and Motor Circuitry Underlying Footshock-Induced Reinstatement of Cocaine-Seeking Behavior

  2004influential reference
• Efferents from medial basal forebrain and hypothalamus in the rat. I. An autoradiographic study of the medial preoptic area

  2004cited by this paper
• The Ventral Tegmental Area Is Required for the Behavioral and Nucleus Accumbens Neuronal Firing Responses to Incentive Cues

  2004cited by this paper
• Brain circuitry and the reinstatement of cocaine-seeking behavior

  2003cited by this paper
• Extended Amygdala and Basal Forebrain

  2003cited by this paper
• Glutamate motivational ensembles in nucleus accumbens: rostrocaudal shell gradients of fear and feeding

  2003cited by this paper
• ANATOMICAL SUBSTRATES OF OREXIN ^ DOPAMINE INTERACTIONS : LATERAL HYPOTHALAMIC PROJECTIONS TO THE VENTRAL TEGMENTAL AREA

  2002cited by this paper
• The caudal sublenticular region/anterior amygdaloid area is the only part of the rat forebrain and mesopontine tegmentum occupied by magnocellular cholinergic neurons that receives outputs from the central division of extended amygdala.

  2002cited by this paper
• Positive and Negative Motivation in Nucleus Accumbens Shell: Bivalent Rostrocaudal Gradients for GABA-Elicited Eating, Taste “Liking”/“Disliking” Reactions, Place Preference/Avoidance, and Fear

  2002cited by this paper
• Limbic-striatal memory systems and drug addiction.

  2002cited by this paper
• Activation of Ventral Tegmental Area Cells by the Bed Nucleus of the Stria Terminalis: A Novel Excitatory Amino Acid Input to Midbrain Dopamine Neurons

  2002cited by this paper
• Potent Regulation of Midbrain Dopamine Neurons by the Bed Nucleus of the Stria Terminalis

  2001cited by this paper
• Fear and Feeding in the Nucleus Accumbens Shell: Rostrocaudal Segregation of GABA-Elicited Defensive Behavior Versus Eating Behavior

  2001cited by this paper
• Projections from the Rat Prefrontal Cortex to the Ventral Tegmental Area: Target Specificity in the Synaptic Associations with Mesoaccumbens and Mesocortical Neurons

  2000cited by this paper
• Distinct Sites of Opiate Reward and Aversion within the Midbrain Identified Using a Herpes Simplex Virus Vector Expressing GluR1

  2000cited by this paper
• Dissociation in Conditioned Dopamine Release in the Nucleus Accumbens Core and Shell in Response to Cocaine Cues and during Cocaine-Seeking Behavior in Rats

  2000cited by this paper
• Dorsal raphe stimulation differentially modulates dopaminergic neurons in the ventral tegmental area and substantia nigra

  2000cited by this paper
• The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking.

  1999cited by this paper
• Afferent connections of the interstitial nucleus of the posterior limb of the anterior commissure and adjacent amygdalostriatal transition area in the rat.

  1999cited by this paper
• A Role for the Bed Nucleus of the Stria Terminalis, But Not the Amygdala, in the Effects of Corticotropin-Releasing Factor on Stress-Induced Reinstatement of Cocaine Seeking

  1999cited by this paper
• Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior.

  1998cited by this paper
• The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity.

  1998cited by this paper
• Efferent projections of the nucleus accumbens in the rat with special reference to subdivision of the nucleus: biotinylated dextran amine study.

  1998cited by this paper
• Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior.

  1998influential reference
• Chemoarchitecture of the rat lateral septal nucleus.

  1997cited by this paper
• Connections of the rat lateral septal complex 1 Published on the World Wide Web on 2 June 1997. 1

  1997cited by this paper
• Self-infusion of GABA(A) antagonists directly into the ventral tegmental area and adjacent regions.

  1997cited by this paper
• Involvement of the ventral tegmental area in locomotion elicited from the nucleus accumbens or ventral pallidum.

  1996cited by this paper
• Stimulation of the prefrontal cortex in the rat induces patterns of activity in midbrain dopaminergic neurons which resemble natural burst events

  1996cited by this paper

• Evaluation of the role of CRFergic neurotransmission in anxiety and BNST neuronal activity in male and female mice exposed to psychosocial stress.

  2025cites this paper
• Oxytocin attenuates demand for cocaine in female rats

  2025influential citation
• The Role of Claustrum in Incubation of Opioid Seeking after Electric Barrier-Induced Voluntary Abstinence in Male and Female Rats

  2025cites this paper
• Fos expression in the periaqueductal gray, but not the ventromedial hypothalamus, is correlated with psychosocial stress-induced cocaine-seeking behavior in rats

  2025cites this paper
• Fos expression in the periaqueductal gray, but not the ventromedial hypothalamus, is correlated with psychosocial stress-induced cocaine-seeking behavior in rats.

  2025cites this paper
• Unravelling the nexus of stroke and dementia: Deciphering the role of secondary neurodegeneration in orchestrating cognitive decline

  2025cites this paper
• Contribution of hypothalamic orexin (hypocretin) circuits to pathologies of motivation

  2024cites this paper
• Ventral pallidum neurons projecting to the ventral tegmental area reinforce but do not invigorate reward-seeking behavior

  2024cites this paper
• Opioid drug seeking after early-life adversity: a role for delta opioid receptors

  2024cites this paper
• Differential rearing alters Fos in the accumbens core and ventral palidum following reinstatement of cocaine seeking in male Sprague-Dawley rats.

  2024cites this paper
• Adolescent THC impacts on mPFC dopamine-mediated cognitive processes in male and female rats

  2024cites this paper
• Role of Piriform Cortex and Its Afferent Projections in Relapse to Fentanyl Seeking after Food Choice-Induced Voluntary Abstinence

  2023cites this paper
• Ventral pallidal regulation of motivated behaviors and reinforcement

  2023cites this paper
• A novel hypothalamic-midbrain circuit for model-based learning

  2023cites this paper
• Alcohol consumption modulates prelimbic cortex response to cocaine following sequential cocaine and alcohol polysubstance use in the rat

  2023cites this paper
• A review of the physiological role of hypocretin in the ventral tegmental area in reward and drug dependence.

  2023cites this paper
• The activity‐regulated cytoskeleton‐associated protein, Arc, functions in the nucleus accumbens shell to limit multiple triggers of cocaine‐seeking behaviour

  2023cites this paper
• The cognitive (lateral) hypothalamus.

  2023cites this paper
• Molecular characteristics and laminar distribution of prefrontal neurons projecting to the mesolimbic system

  2022cites this paper
• Microstructural Impairments in a Topologically Distinct Prefrontal-Habenular Connection in Cocaine Addiction

  2022cites this paper
• Glucagon-like peptide-1 receptors in nucleus accumbens, ventral hippocampus, and lateral septum reduce alcohol reinforcement in mice.

  2022cites this paper
• The role of the bed nucleus of the stria terminalis in the motivational control of instrumental action

  2022cites this paper
• Enduring disruption of reward and stress circuit activities by early-life adversity in male rats

  2022cites this paper
• Neural correlates and potential targets for the contribution of orexin to addiction in cortical and subcortical areas.

  2022cites this paper
• Prefrontal-habenular microstructural impairments in human cocaine and heroin addiction.

  2022cites this paper
• Ventral pallidum GABA neurons bidirectionally control opioid relapse across rat behavioral models

  2022cites this paper
• Transcriptome profiling of the ventral pallidum reveals a role for pallido-thalamic neurons in cocaine reward

  2021cites this paper
• Dopamine Circuit Mechanisms of Addiction-Like Behaviors

  2021cites this paper
• Lateral Septum as a Nexus for Mood, Motivation, and Movement.

  2021cites this paper
• Dopamine and relapse to drug seeking

  2021influential citation
• Dynamic Changes of Arc Expression in Dorsal Striatum of Mice After Self-Administration of Sucrose

  2021cites this paper
• Intermittent self‐administration of fentanyl induces a multifaceted addiction state associated with persistent changes in the orexin system

  2020cites this paper
• Behavioral and Neurobiological Mechanisms of Pavlovian and Instrumental Extinction Learning.

  2020cites this paper
• Chronic intermittent ethanol exposure dysregulates a GABAergic microcircuit in the bed nucleus of the stria terminalis.

  2020cites this paper
• Role of Projections between Piriform Cortex and Orbitofrontal Cortex in Relapse to Fentanyl Seeking after Palatable Food Choice-Induced Voluntary Abstinence

  2020cites this paper
• Sex Differences in Demand for Highly Palatable Foods: Role of the Orexin System

  2020cites this paper
• Pharmacokinetic, behavioral, and brain activity effects of Δ9-tetrahydrocannabinol in adolescent male and female rats

  2020cites this paper
• Activation of medial hypothalamic orexin neurons during a Go/No-Go task.

  2020cites this paper
• Intermittent self-administration of fentanyl induces a multifaceted addiction state associated with persistent changes in the orexin system

  2020cites this paper
• Cell type- and pathway-specific synaptic regulation of orexin neurocircuitry.

  2020cites this paper
• Prelimbic cortical projections to rostromedial tegmental nucleus play a suppressive role in cue-induced reinstatement of cocaine seeking

  2020cites this paper
• Complementary Roles for Ventral Pallidum Cell Types and Their Projections in Relapse

  2019cites this paper
• Persistent effects of the orexin-1 receptor antagonist SB-334867 on motivation for the fast acting opioid remifentanil

  2019cites this paper
• The number of lateral hypothalamus orexin/hypocretin neurons contributes to individual differences in cocaine demand

  2019cites this paper
• Characterization of the relaxin family peptide receptor 3 system in the mouse bed nucleus of the stria terminalis

  2019cites this paper
• Chemogenetic modulation of accumbens direct or indirect pathways bidirectionally alters reinstatement of heroin-seeking in high- but not low-risk rats

  2019cites this paper
• Examination of the Role of Neuroimmune Signaling in Drug Addiction

  2019cites this paper
• The effects of reward devaluation on cue-evoked modulation of sucrose seeking and neuronal ensemble plasticity in nucleus accumbens

  2019cites this paper
• Probabilistic

  2019cites this paper
• From controlled to compulsive drug-taking: The role of the habenula in addiction.

  2019cites this paper
• Adolescent social isolation increases cocaine seeking in male and female mice

  2019cites this paper
• Preproenkephalin‐expressing ventral pallidal neurons control inhibitory avoidance learning

  2019cites this paper
• Ethanol-induced conditioned place preference and aversion differentially alter plasticity in the bed nucleus of stria terminalis

  2019cites this paper
• Central GLP-1 receptors: Novel molecular targets for cocaine use disorder.

  2019cites this paper
• Early-life adversity facilitates acquisition of cocaine self-administration and induces persistent anhedonia

  2018cites this paper
• The weaning period promotes alterations in the orexin neuronal population of rats in a suckling-dependent manner

  2018cites this paper
• Neuropeptide Y and orexin immunoreactivity in the sparrow brain coincide with seasonal changes in energy balance and steroids

  2018cites this paper
• Common neurocircuitry mediating drug and fear relapse in preclinical models

  2018cites this paper
• Orexin-1 receptor signaling in ventral pallidum mediates demand for the opioid remifentanil

  2018cites this paper
• Prelimbic cortex is a common brain area activated during cue‐induced reinstatement of cocaine and heroin seeking in a polydrug self‐administration rat model

  2018cites this paper
• Dorsal Hippocampus Drives Context-Induced Cocaine Seeking via Inputs to Lateral Septum

  2018cites this paper
• Chemogenetic Manipulations of Ventral Tegmental Area Dopamine Neurons Reveal Multifaceted Roles in Cocaine Abuse

  2018cites this paper
• Mapping a Pup-responsive Pathway from the Medial Preoptic Area to the Ventral Tegmental Area.

  2018influential citation
• Learning in alcohol dependence Pavlovian-to-instrumental transfer in alcohol dependence and relapse risk

  2018cites this paper
• Adolescent Social Isolation Increases Vulnerability to Cocaine

  2018cites this paper
• The intersection of stress and reward: BNST modulation of aversive and appetitive states

  2018cites this paper
• Circuit directionality for motivation: lateral accumbens-pallidum, but not pallidum-accumbens, connections regulate motivational attraction to reward cues

  2018cites this paper
• Modeling cocaine relapse in rodents: Behavioral considerations and circuit mechanisms

  2018influential citation
• Heterogeneous neuronal activity in the lateral habenula after short‐ and long‐term cocaine self‐administration in rats

  2018cites this paper
• Attenuated cocaine-seeking after oxytocin administration in male and female rats

  2018cites this paper
• 2 Orexin Signaling and Self-Administration Behavior 2 . 1 Traditional Self-Administration Models

  2018cites this paper
• Motor skill learning and reward consumption differentially affect VTA activation

  2018cites this paper
• A Focus on Reward Prediction and the Lateral Habenula: Functional Alterations and the Behavioral Outcomes Induced by Drugs of Abuse

  2018influential citation
• What does the Fos say? Using Fos-based approaches to understand the contribution of stress to substance use disorders

  2018cites this paper
• Modulation des Kontrollnetzwerkes für Nahrungsaufnahme: Eine kombinierte fMRT- und rTMS-Studie an gesunden Probanden

  2018cites this paper
• Cocaine Interaction with Dopamine Transporter in the Prefrontal Cortex and Beyond

  2018cites this paper
• The nucleus accumbens shell in reinstatement and extinction of drug seeking

  2018cites this paper
• Cued Reinstatement of Cocaine but Not Sucrose Seeking Is Dependent on Dopamine Signaling in Prelimbic Cortex and Is Associated with Recruitment of Prelimbic Neurons That Project to Contralateral Nucleus Accumbens Core

  2017cites this paper
• Oxytocin Acts in Nucleus Accumbens to Attenuate Methamphetamine Seeking and Demand.

  2017influential citation
• Deep Brain Stimulation: A Possible Therapeutic Technique for Treating Refractory Alcohol and Drug Addiction Behaviors

  2017cites this paper
• Cocaine Seeking During Initial Abstinence Is Driven by Noradrenergic and Serotonergic Signaling in Hippocampus in a Sex-Dependent Manner

  2017cites this paper
• Ethanol‐seeking behavior is expressed directly through an extended amygdala to midbrain neural circuit

  2017influential citation
• The lateral habenula and alcohol: Role of glutamate and M‐type potassium channels

  2017cites this paper
• The Contribution of the Amygdala to Reward-Related Learning and Extinction

  2017influential citation
• The bed nucleus of the stria terminalis in drug‐associated behavior and affect: A circuit‐based perspective

  2017cites this paper
• The Role of the Habenulomesencephalic Circuit in Cocaine Addiction

  2017cites this paper
• How contexts promote and prevent relapse to drug seeking

  2017cites this paper
• The habenula in psychiatric disorders: More than three decades of translational investigation

  2017cites this paper
• Cue‐induced reinstatement of alcohol‐seeking behavior is associated with increased CaMKII T286 phosphorylation in the reward pathway of mice

  2017cites this paper
• Palatable food self‐administration and reinstatement are not affected by dual orexin receptor antagonism

  2017cites this paper
• Influence of preoptic estradiol on behavioral and neural response to cocaine in female Sprague-Dawley rats

  2017cites this paper
• Pharmacological modulation of lateral habenular dopamine D2 receptors alters the anxiogenic response to cocaine in a runway model of drug self-administration.

  2016cites this paper
• Frontostriatal Circuit Dynamics Correlate with Cocaine Cue-Evoked Behavioral Arousal during Early Abstinence123

  2016cites this paper
• Animal models of drug relapse and craving: From drug priming-induced reinstatement to incubation of craving after voluntary abstinence.

  2016cites this paper
• Prelimbic to Accumbens Core Pathway Is Recruited in a Dopamine-Dependent Manner to Drive Cued Reinstatement of Cocaine Seeking

  2016influential citation
• Ventral Tegmental Area Afferents and Drug-Dependent Behaviors

  2016influential citation
• Adolescent

  2016cites this paper
• Ventral Pallidum Output Pathways in Context-Induced Reinstatement of Alcohol Seeking

  2016cites this paper
• Toward a systems-oriented approach to the role of the extended amygdala in adaptive responding.

  2016cites this paper
• Orexin/hypocretin neuron activation is correlated with alcohol seeking and preference in a topographically specific manner

  2016cites this paper