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Article ; Online: Serotonin Signaling in Hippocampus during Initial Cocaine Abstinence Drives Persistent Drug Seeking.

Kohtz, Amy S / Zhao, Joshua / Aston-Jones, Gary

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

2024 Volume 44, Issue 17

Abstract: The initiation of abstinence after chronic drug self-administration is stressful. Cocaine-seeking behavior on the first day of the absence of the expected drug (Extinction Day 1, ED1) is reduced by blocking 5-HT signaling in dorsal hippocampal cornu ... ...

Abstract	The initiation of abstinence after chronic drug self-administration is stressful. Cocaine-seeking behavior on the first day of the absence of the expected drug (Extinction Day 1, ED1) is reduced by blocking 5-HT signaling in dorsal hippocampal cornu ammonis 1 (CA1) in both male and female rats. We hypothesized that the experience of ED1 can substantially influence later relapse behavior and that dorsal raphe (DR) serotonin (5-HT) input to CA1 may be involved. We inhibited 5-HT
MeSH term(s)	Animals ; Male ; Drug-Seeking Behavior/physiology ; Drug-Seeking Behavior/drug effects ; Rats ; Serotonin/metabolism ; Female ; Cocaine/administration & dosage ; Cocaine/pharmacology ; Hippocampus/metabolism ; Hippocampus/drug effects ; Pyridines/pharmacology ; Serotonin Antagonists/pharmacology ; Signal Transduction/drug effects ; Signal Transduction/physiology ; Piperazines/pharmacology ; Rats, Sprague-Dawley ; Cocaine-Related Disorders/metabolism ; Cocaine-Related Disorders/psychology ; Self Administration ; Extinction, Psychological/drug effects ; Extinction, Psychological/physiology ; Receptor, Serotonin, 5-HT1B/metabolism ; CA1 Region, Hippocampal/drug effects ; CA1 Region, Hippocampal/metabolism ; Oxadiazoles
Chemical Substances	Serotonin (333DO1RDJY) ; Cocaine (I5Y540LHVR) ; N-(2-(4-(2-methoxyphenyl)-1-piperazinyl)ethyl)-N-(2-pyridinyl)cyclohexanecarboxamide (71IH826FEG) ; Pyridines ; Serotonin Antagonists ; Piperazines ; GR 127935 (2LLH6CEB40) ; Receptor, Serotonin, 5-HT1B ; Oxadiazoles
Language	English
Publishing date	2024-04-24
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.1505-21.2024
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Article ; Online: Orexin Reserve: A Mechanistic Framework for the Role of Orexins (Hypocretins) in Addiction.

James, Morgan H / Aston-Jones, Gary

Biological psychiatry

2022 Volume 92, Issue 11, Page(s) 836–844

Abstract: In 2014, we proposed that orexin signaling transformed motivationally relevant states into adaptive behavior directed toward exploiting an opportunity or managing a threat, a process we referred to as motivational activation. Advancements in animal ... ...

Abstract	In 2014, we proposed that orexin signaling transformed motivationally relevant states into adaptive behavior directed toward exploiting an opportunity or managing a threat, a process we referred to as motivational activation. Advancements in animal models since then have permitted higher-resolution measurements of motivational states; in particular, the behavioral economics approach for studying drug demand characterizes conditions that lead to the enhanced motivation that underlies addiction. This motivational plasticity is paralleled by persistently increased orexin expression in a topographically specific manner-a finding confirmed across species, including in humans. Normalization of orexin levels also reduces drug motivation in addiction models. These new advancements lead us to update our proposed framework for the orexin function. We now propose that the capacity of orexin neurons to exhibit dynamic shifts in peptide production contributes to their role in adaptive motivational regulation and that this is achieved via a pool of reserve orexin neurons. This reserve is normally bidirectionally recruited to permit motivational plasticity that promotes flexible, adaptive behavior. In pathological states such as addiction, however, we propose that the orexin system loses capacity to adaptively adjust peptide production, resulting in focused hypermotivation for drug, driven by aberrantly and persistently high expression in the orexin reserve pool. This mechanistic framework has implications for the understanding and treatment of several psychiatric disorders beyond addiction, particularly those characterized by motivational dysfunction.
MeSH term(s)	Animals ; Humans ; Orexins ; Neuropeptides/metabolism ; Intracellular Signaling Peptides and Proteins ; Behavior, Addictive/metabolism ; Motivation ; Orexin Receptors
Chemical Substances	Orexins ; Neuropeptides ; Intracellular Signaling Peptides and Proteins ; Orexin Receptors
Language	English
Publishing date	2022-07-03
Publishing country	United States
Document type	Journal Article ; Review ; Research Support, N.I.H., Extramural
ZDB-ID	209434-4
ISSN	1873-2402 ; 0006-3223
ISSN (online)	1873-2402
ISSN	0006-3223
DOI	10.1016/j.biopsych.2022.06.027
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Article ; Online: Prelimbic and infralimbic medial prefrontal cortex neuron activity signals cocaine seeking variables across multiple timescales.

Moorman, David E / Aston-Jones, Gary

Psychopharmacology

2022 Volume 240, Issue 3, Page(s) 575–594

Abstract: Rationale and objectives: The prefrontal cortex is critical for execution and inhibition of reward seeking. Neural manipulation of rodent medial prefrontal cortex (mPFC) subregions differentially impacts execution and inhibition of cocaine seeking. ... ...

Abstract	Rationale and objectives: The prefrontal cortex is critical for execution and inhibition of reward seeking. Neural manipulation of rodent medial prefrontal cortex (mPFC) subregions differentially impacts execution and inhibition of cocaine seeking. Dorsal, or prelimbic (PL), and ventral, or infralimbic (IL) mPFC are implicated in cocaine seeking or extinction of cocaine seeking, respectively. This differentiation is not seen across all studies, indicating that further research is needed to understand specific mPFC contributions to drug seeking. Methods: We recorded neuronal activity in mPFC subregions during cocaine self-administration, extinction, and cue- and cocaine-induced reinstatement of cocaine seeking. Results: Both PL and IL neurons were phasically responsive around lever presses during cocaine self-administration, and activity in both areas was reduced during extinction. During both cue- and, to a greater extent, cocaine-induced reinstatement, PL neurons exhibited significantly elevated responses, in line with previous studies demonstrating a role for the region in relapse. The enhanced PL signaling in cocaine-induced reinstatement was driven by strong excitation and inhibition in different groups of neurons. Both of these response types were stronger in PL vs. IL neurons. Finally, we observed tonic changes in activity in all tasks phases, reflecting both session-long contextual modulation as well as minute-to-minute activity changes that were highly correlated with brain cocaine levels and motivation associated with cocaine seeking. Conclusions: Although some differences were observed between PL and IL neuron activity across sessions, we found no evidence of a go/stop dichotomy in PL/IL function. Instead, our results demonstrate temporally heterogeneous prefrontal signaling during cocaine seeking and extinction in both PL and IL, revealing novel and complex functions for both regions during these behaviors. This combination of findings argues that mPFC neurons, in both PL and IL, provide multifaceted contributions to the regulation of drug seeking and addiction.
MeSH term(s)	Cocaine/pharmacology ; Cues ; Prefrontal Cortex/physiology ; Neurons ; Reward ; Extinction, Psychological/physiology ; Drug-Seeking Behavior/physiology ; Self Administration
Chemical Substances	Cocaine (I5Y540LHVR)
Language	English
Publishing date	2022-12-05
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/s00213-022-06287-2
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Article ; Online: Novelty preference does not predict trait cocaine behaviors in male rats.

O'Connor, Shayna L / Aston-Jones, Gary / James, Morgan H

Addiction neuroscience

2022 Volume 2

Abstract: Heightened novelty seeking is a risk factor for the initiation of drug use and development of substance use disorders. In rats, novelty seeking can be examined by assessing preference for a novel environment. Some evidence indicates that high novelty ... ...

Abstract	Heightened novelty seeking is a risk factor for the initiation of drug use and development of substance use disorders. In rats, novelty seeking can be examined by assessing preference for a novel environment. Some evidence indicates that high novelty preferring (HNP) rats have higher drug intake compared to low novelty preferring (LNP) rats, although these data are mixed. Moreover, the extent to which the HNP phenotype can predict other initial drug behaviors, including economic demand for cocaine, has not been tested. Here, we screened a cohort (n=60) of male rats for novelty preference and several subsequent cocaine behaviors, including locomotor reactivity to a cocaine priming injection, acquisition of cocaine self-administration, as well as cocaine demand using a within-session behavioral economics procedure. Novelty preference did not correlate with cocaine behaviors, nor were there any differences between HNP and LNP rats identified using a median split strategy. Moreover, regression analyses indicated that novelty preference did not have predictive utility for any of the cocaine behaviors tested. Thus, the extent to which the novelty preference trait can predict initial cocaine-related behaviors in male rats may be limited. This is in contrast to the novel locomotor reactivity phenotype, which is strongly linked with initial cocaine intake, indicating that these traits are distinct and differentially predict cocaine behaviors in rats.
Language	English
Publishing date	2022-03-23
Publishing country	Netherlands
Document type	Journal Article
ISSN	2772-3925
ISSN (online)	2772-3925
DOI	10.1016/j.addicn.2022.100013
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Article ; Online: Introduction to the Special Issue: "Making orexin-based therapies for addiction a reality: What are the steps from here?"

James, Morgan H / Aston-Jones, Gary

Brain research

2020 Volume 1731, Page(s) 146665

MeSH term(s)	Animals ; Behavior, Addictive/drug therapy ; Behavior, Addictive/physiopathology ; Brain/drug effects ; Brain/physiopathology ; Humans ; Motivation/drug effects ; Motivation/physiology ; Neurons/drug effects ; Neurons/physiology ; Orexin Receptor Antagonists/administration & dosage ; Substance-Related Disorders/drug therapy ; Substance-Related Disorders/physiopathology
Chemical Substances	Orexin Receptor Antagonists
Language	English
Publishing date	2020-01-10
Publishing country	Netherlands
Document type	Editorial ; Introductory Journal Article
ZDB-ID	1200-2
ISSN	1872-6240 ; 0006-8993
ISSN (online)	1872-6240
ISSN	0006-8993
DOI	10.1016/j.brainres.2020.146665
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Article ; Online: Intermittent self-administration of fentanyl induces a multifaceted addiction state associated with persistent changes in the orexin system.

Fragale, Jennifer E / James, Morgan H / Aston-Jones, Gary

Addiction biology

2020 Volume 26, Issue 3, Page(s) e12946

Abstract: The orexin (hypocretin) system plays a critical role in motivated drug taking. Cocaine self-administration with the intermittent access (IntA) procedure produces a robust addiction-like state that is orexin-dependent. Here, we sought to determine the ... ...

Abstract	The orexin (hypocretin) system plays a critical role in motivated drug taking. Cocaine self-administration with the intermittent access (IntA) procedure produces a robust addiction-like state that is orexin-dependent. Here, we sought to determine the role of the orexin system in opioid addiction using IntA self-administration of fentanyl. Different groups of male rats were either given continuous access in 1-h period (short access [ShA]), 6-h period (long access [LgA]), or IntA (5 min of access separated by 25 min of no access for 6 h) to fentanyl for 14 days. IntA produced a greater escalation of fentanyl intake, increased motivation for fentanyl on a behavioral economics task, persistent drug seeking during abstinence, and stronger cue-induced reinstatement compared with rats given ShA or LgA. We found that addiction behaviors induced by IntA to fentanyl were reversed by the orexin-1 receptor antagonist SB-334867. IntA to fentanyl was also associated with a persistent increase in the number of orexin neurons. Together, these results indicate that the IntA model is a useful tool in the study of opioid addiction and that the orexin system is critical for the maintenance of addiction behaviors induced by IntA self-administration of fentanyl.
MeSH term(s)	Animals ; Benzoxazoles/pharmacology ; Drug-Seeking Behavior/drug effects ; Economics, Behavioral ; Fentanyl/pharmacology ; Male ; Motivation ; Naphthyridines/pharmacology ; Orexin Receptors ; Orexins/antagonists & inhibitors ; Orexins/genetics ; Orexins/physiology ; Rats ; Rats, Sprague-Dawley ; Self Administration ; Urea/analogs & derivatives ; Urea/pharmacology
Chemical Substances	1-(2-methylbenzoxazol-6-yl)-3-(1,5)naphthyridin-4-yl urea ; Benzoxazoles ; Hcrt protein, rat ; Naphthyridines ; Orexin Receptors ; Orexins ; Urea (8W8T17847W) ; Fentanyl (UF599785JZ)
Language	English
Publishing date	2020-08-14
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1324314-7
ISSN	1369-1600 ; 1355-6215
ISSN (online)	1369-1600
ISSN	1355-6215
DOI	10.1111/adb.12946
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Article ; Online: Hormonal milieu drives economic demand for cocaine in female rats.

Kohtz, Amy S / Lin, Belle / Davies, Hannah / Presker, Mark / Aston-Jones, Gary

Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology

2022 Volume 47, Issue 8, Page(s) 1484–1492

Abstract: There are substantial sex differences in drug abuse, and a key feature of cocaine addiction is pathologically high motivation for drug. We investigated the role of ovarian hormones on cocaine demand in female rats using a within-session threshold ... ...

Abstract	There are substantial sex differences in drug abuse, and a key feature of cocaine addiction is pathologically high motivation for drug. We investigated the role of ovarian hormones on cocaine demand in female rats using a within-session threshold behavioral economics (BE) procedure, which allows us to compare motivation for drug across hormonal states and sex while controlling for differences in dose and intake. This approach quantifies demand elasticity (α) and free consumption (Q
MeSH term(s)	Animals ; Cocaine ; Cocaine-Related Disorders ; Economics, Behavioral ; Female ; Male ; Rats ; Rats, Sprague-Dawley ; Self Administration
Chemical Substances	Cocaine (I5Y540LHVR)
Language	English
Publishing date	2022-03-25
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	639471-1
ISSN	1740-634X ; 0893-133X
ISSN (online)	1740-634X
ISSN	0893-133X
DOI	10.1038/s41386-022-01304-6
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Article ; Online: The sensation seeking trait confers a dormant susceptibility to addiction that is revealed by intermittent cocaine self-administration in rats.

O'Connor, Shayna L / Aston-Jones, Gary / James, Morgan H

Neuropharmacology

2021 Volume 195, Page(s) 108566

Abstract: Heightened sensation seeking is associated with an increased risk of substance use disorder in clinical populations. In rats, sensation seeking is often examined by measuring locomotor reactivity to a novel environment. So-called high responders (HR) ... ...

Abstract	Heightened sensation seeking is associated with an increased risk of substance use disorder in clinical populations. In rats, sensation seeking is often examined by measuring locomotor reactivity to a novel environment. So-called high responders (HR) acquire self-administration of psychostimulants more quickly and consume higher amounts of drug compared to low responder (LR) rats, indicating that the HR trait might confer a stronger addiction propensity. However, studies of addiction-like behaviors in HR vs LR rats have typically utilized self-administration paradigms that do not dissociate individual differences in the hedonic/reinforcing and motivational properties of a drug. Moreover, little attention has been given to whether HR rats are more susceptible to drug-access conditions that promote a state-dependent addiction phenotype. We report that on a behavioral economics task, HR rats have higher preferred brain-cocaine levels compared to LR rats but do not differ with respect to their demand elasticity for cocaine. In contrast, when tested on an intermittent access schedule of cocaine self-administration, which has been shown to promote several addiction-related endophenotypes, HR rats exhibit greater escalation of intake and more drastic reductions in cocaine demand elasticity. Together, these data indicate that the HR trait does not confer higher extant addiction behavior, but rather that this phenotype is associated with a propensity for addiction that remains dormant until it is actuated by intermittent drug intake. These findings reveal a 'trait' (HR) by 'state' (intermittent drug intake) interaction that produces a strong addiction-like phenotype. This article is part of the special issue on 'Vulnerabilities to Substance Abuse'.
MeSH term(s)	Animals ; Behavior, Animal/drug effects ; Cocaine/administration & dosage ; Cocaine-Related Disorders/physiopathology ; Dopamine Uptake Inhibitors/administration & dosage ; Drug-Seeking Behavior/drug effects ; Male ; Motor Activity/drug effects ; Rats ; Rats, Sprague-Dawley ; Self Administration
Chemical Substances	Dopamine Uptake Inhibitors ; Cocaine (I5Y540LHVR)
Language	English
Publishing date	2021-04-20
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	218272-5
ISSN	1873-7064 ; 0028-3908
ISSN (online)	1873-7064
ISSN	0028-3908
DOI	10.1016/j.neuropharm.2021.108566
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Article ; Online: Introduction to the special issue: "Role of corticostriatal circuits in addiction".

Aston-Jones, Gary

Brain research

2015 Volume 1628, Issue Pt A, Page(s) 1

MeSH term(s)	Animals ; Behavior, Addictive/physiopathology ; Behavior, Addictive/therapy ; Cerebral Cortex/physiopathology ; Corpus Striatum/physiopathology ; Humans ; Neural Pathways/physiopathology ; Substance-Related Disorders/physiopathology ; Substance-Related Disorders/therapy
Language	English
Publishing date	2015-12-02
Publishing country	Netherlands
Document type	Editorial ; Introductory Journal Article
ZDB-ID	1200-2
ISSN	1872-6240 ; 0006-8993
ISSN (online)	1872-6240
ISSN	0006-8993
DOI	10.1016/j.brainres.2015.10.046
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Article ; Online: Lateral septum inhibition reduces motivation for cocaine: Reversal by diazepam.

Pantazis, Caroline B / Aston-Jones, Gary

Addiction biology

2019 Volume 25, Issue 2, Page(s) e12742

Abstract: The lateral septum (LS) is a brain region implicated in motivation, addiction, anxiety, and affect. We recently found that LS is necessary for cocaine-seeking behaviors including conditioned place preference and reinstatement of extinguished drug seeking, ...

Abstract	The lateral septum (LS) is a brain region implicated in motivation, addiction, anxiety, and affect. We recently found that LS is necessary for cocaine-seeking behaviors including conditioned place preference and reinstatement of extinguished drug seeking, which involve LS input to limbic regions including ventral tegmental area (VTA) and orexin neurons in hypothalamus. Here, we microinjected baclofen-muscimol (B-M) in LS prior to testing in a behavioral economics (BE) paradigm. We found that intra-LS B-M decreased motivation (increased demand elasticity; α) for cocaine, but did not change consumption at low effort (Q
MeSH term(s)	Animals ; Behavior, Animal/drug effects ; Cocaine/pharmacology ; Cocaine-Related Disorders/physiopathology ; Diazepam/pharmacology ; Disease Models, Animal ; Dopamine Uptake Inhibitors/pharmacology ; GABA Modulators/pharmacology ; Male ; Motivation/drug effects ; Rats ; Rats, Sprague-Dawley ; Septal Nuclei/drug effects ; Septal Nuclei/physiopathology
Chemical Substances	Dopamine Uptake Inhibitors ; GABA Modulators ; Cocaine (I5Y540LHVR) ; Diazepam (Q3JTX2Q7TU)
Language	English
Publishing date	2019-03-21
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1324314-7
ISSN	1369-1600 ; 1355-6215
ISSN (online)	1369-1600
ISSN	1355-6215
DOI	10.1111/adb.12742
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