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Article ; Online: A large-scale c-Fos brain mapping study on extinction of cocaine-primed reinstatement.

Lenoir, Magalie / Engeln, Michel / Navailles, Sylvia / Girardeau, Paul / Ahmed, Serge H

Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology

2024

Abstract: Individuals with cocaine addiction can experience many craving episodes and subsequent relapses, which represents the main obstacle to recovery. Craving is often favored when abstinent individuals ingest a small dose of cocaine, encounter cues associated ...

Abstract	Individuals with cocaine addiction can experience many craving episodes and subsequent relapses, which represents the main obstacle to recovery. Craving is often favored when abstinent individuals ingest a small dose of cocaine, encounter cues associated with drug use or are exposed to stressors. Using a cocaine-primed reinstatement model in rat, we recently showed that cocaine-conditioned interoceptive cues can be extinguished with repeated cocaine priming in the absence of drug reinforcement, a phenomenon we called extinction of cocaine priming. Here, we applied a large-scale c-Fos brain mapping approach following extinction of cocaine priming in male rats to identify brain regions implicated in processing the conditioned interoceptive stimuli of cocaine priming. We found that cocaine-primed reinstatement is associated with increased c-Fos expression in key brain regions (e.g., dorsal and ventral striatum, several prefrontal areas and insular cortex), while its extinction mostly disengages them. Moreover, while reinstatement behavior was correlated with insular and accumbal activation, extinction of cocaine priming implicated parts of the ventral pallidum, the mediodorsal thalamus and the median raphe. These brain patterns of activation and inhibition suggest that after repeated priming, interoceptive signals lose their conditioned discriminative properties and that action-outcome associations systems are mobilized in search for new contingencies, a brain state that may predispose to rapid relapse.
Language	English
Publishing date	2024-04-25
Publishing country	England
Document type	Journal Article
ZDB-ID	639471-1
ISSN	1740-634X ; 0893-133X
ISSN (online)	1740-634X
ISSN	0893-133X
DOI	10.1038/s41386-024-01867-6
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Article ; Online: Large-scale brain correlates of sweet versus cocaine reward in rats.

Lenoir, Magalie / Navailles, Sylvia / Vandaele, Youna / Vouillac-Mendoza, Caroline / Guillem, Karine / Ahmed, Serge H

The European journal of neuroscience

2022 Volume 57, Issue 3, Page(s) 423–439

Abstract: Cocaine induces many supranormal changes in neuronal activity in the brain, notably in learning- and reward-related regions, in comparison with nondrug rewards-a difference that is thought to contribute to its relatively high addictive potential. However, ...

Abstract	Cocaine induces many supranormal changes in neuronal activity in the brain, notably in learning- and reward-related regions, in comparison with nondrug rewards-a difference that is thought to contribute to its relatively high addictive potential. However, when facing a choice between cocaine and a nondrug reward (e.g., water sweetened with saccharin), most rats do not choose cocaine, as one would expect from the extent and magnitude of its global activation of the brain, but instead choose the nondrug option. We recently showed that cocaine, though larger in magnitude, is also an inherently more delayed reward than sweet water, thereby explaining why it has less value during choice and why rats opt for the more immediate nondrug option. Here, we used a large-scale Fos brain mapping approach to measure brain responses to each option in saccharin-preferring rats, with the hope to identify brain regions whose activity may explain the preference for the nondrug option. In total, Fos expression was measured in 142 brain levels corresponding to 52 brain subregions and composing 5 brain macrosystems. Overall, our findings confirm in rats with a preference for saccharin that cocaine induces more global brain activation than the preferred nondrug option does. Only very few brain regions were uniquely activated by saccharin. They included regions involved in taste processing (i.e., anterior gustatory cortex) and also regions involved in processing reward delay and intertemporal choice (i.e., some components of the septohippocampal system and its connections with the lateral habenula).
MeSH term(s)	Rats ; Animals ; Cocaine/pharmacology ; Saccharin/pharmacology ; Taste ; Rats, Wistar ; Conditioning, Operant ; Reward ; Brain ; Water
Chemical Substances	Cocaine (I5Y540LHVR) ; Saccharin (FST467XS7D) ; Water (059QF0KO0R)
Language	English
Publishing date	2022-12-13
Publishing country	France
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	645180-9
ISSN	1460-9568 ; 0953-816X
ISSN (online)	1460-9568
ISSN	0953-816X
DOI	10.1111/ejn.15879
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Article ; Online: Probing the decision-making mechanisms underlying choice between drug and nondrug rewards in rats.

Vandaele, Youna / Lenoir, Magalie / Vouillac-Mendoza, Caroline / Guillem, Karine / Ahmed, Serge H

eLife

2021 Volume 10

Abstract: Delineating the decision-making mechanisms underlying choice between drug and nondrug rewards remains a challenge. This study adopts an original approach to probe these mechanisms by comparing response latencies during sampling versus choice trials. ... ...

Abstract	Delineating the decision-making mechanisms underlying choice between drug and nondrug rewards remains a challenge. This study adopts an original approach to probe these mechanisms by comparing response latencies during sampling versus choice trials. While lengthening of latencies during choice is predicted in a deliberative choice model (DCM), the race-like response competition mechanism postulated by the Sequential choice model (SCM) predicts a shortening of latencies during choice compared to sampling. Here, we tested these predictions by conducting a retrospective analysis of cocaine-versus-saccharin choice experiments conducted in our laboratory. We found that rats engage deliberative decision-making mechanisms after limited training, but adopt a SCM-like response selection mechanism after more extended training, while their behavior is presumably habitual. Thus, the DCM and SCM may not be general models of choice, as initially formulated, but could be dynamically engaged to control choice behavior across early and extended training.
MeSH term(s)	Animals ; Choice Behavior/drug effects ; Cocaine/administration & dosage ; Male ; Rats/physiology ; Rats/psychology ; Rats, Wistar ; Retrospective Studies ; Saccharin/administration & dosage
Chemical Substances	Saccharin (FST467XS7D) ; Cocaine (I5Y540LHVR)
Language	English
Publishing date	2021-04-26
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.64993
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Article ; Online: Qu’apporte la neurobiologie aux addictions ?

Lenoir, Magalie / Noble, Florence

Presse medicale (Paris, France : 1983)

2016 Volume 45, Issue 12 Pt 1, Page(s) 1096–1101

Abstract: Addictions are multifactorial, and there are no experimental models replicating all aspects of this pathology. The development of animal models reproducing the clinical symptoms of addictions allows significant advances in the knowledge of the ... ...

Title translation	What brings neurobiology to addictions?
Abstract	Addictions are multifactorial, and there are no experimental models replicating all aspects of this pathology. The development of animal models reproducing the clinical symptoms of addictions allows significant advances in the knowledge of the neurobiological processes involved in addiction. Preclinical data highlight different neuroadaptations according to the routes of administration, speeds of injection and frequencies of exposure to drugs of abuse. The neuroadaptations induced by an exposure to drugs of abuse follow dynamic processes in time. Despite significant progresses in the knowledge of neurobiology of addictions allowing to propose new therapeutic targets, the passage of new drugs in clinical is often disappointing. The lack of treatment efficacy reported in clinical trials is probably due to a very important heterogeneity of patients with distinct biological and genetic factors, but also with different patterns of consumption that can lead to different neuroadaptations, as clearly observed in preclinical studies.
MeSH term(s)	Animals ; Disease Models, Animal ; Humans ; Neurobiology ; Substance-Related Disorders/diagnosis ; Substance-Related Disorders/therapy
Language	French
Publishing date	2016-12
Publishing country	France
Document type	Journal Article
ZDB-ID	120943-7
ISSN	2213-0276 ; 0032-7867 ; 0755-4982 ; 0301-1518
ISSN (online)	2213-0276
ISSN	0032-7867 ; 0755-4982 ; 0301-1518
DOI	10.1016/j.lpm.2016.02.021
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Article ; Online: Probing the decision-making mechanisms underlying choice between drug and nondrug rewards in rats

Youna Vandaele / Magalie Lenoir / Caroline Vouillac-Mendoza / Karine Guillem / Serge H Ahmed

eLife, Vol

2021 Volume 10

Abstract	Delineating the decision-making mechanisms underlying choice between drug and nondrug rewards remains a challenge. This study adopts an original approach to probe these mechanisms by comparing response latencies during sampling versus choice trials. While lengthening of latencies during choice is predicted in a deliberative choice model (DCM), the race-like response competition mechanism postulated by the Sequential choice model (SCM) predicts a shortening of latencies during choice compared to sampling. Here, we tested these predictions by conducting a retrospective analysis of cocaine-versus-saccharin choice experiments conducted in our laboratory. We found that rats engage deliberative decision-making mechanisms after limited training, but adopt a SCM-like response selection mechanism after more extended training, while their behavior is presumably habitual. Thus, the DCM and SCM may not be general models of choice, as initially formulated, but could be dynamically engaged to control choice behavior across early and extended training.
Keywords	deliberative choice model ; sequential choice model ; cocaine ; saccharin ; decision-making ; Medicine ; R ; Science ; Q ; Biology (General) ; QH301-705.5
Subject code	150
Language	English
Publishing date	2021-04-01T00:00:00Z
Publisher	eLife Sciences Publications Ltd
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Intravenous nicotine injection induces rapid, experience-dependent sensitization of glutamate release in the ventral tegmental area and nucleus accumbens.

Lenoir, Magalie / Kiyatkin, Eugene A

Journal of neurochemistry

2013 Volume 127, Issue 4, Page(s) 541–551

Abstract: Although numerous data suggest that glutamate (GLU) is involved in mediating the neural effects of nicotine, direct data on nicotine-induced changes in GLU release are still lacking. Here, we used high-speed amperometry with enzyme-based GLU and enzyme- ... ...

Abstract	Although numerous data suggest that glutamate (GLU) is involved in mediating the neural effects of nicotine, direct data on nicotine-induced changes in GLU release are still lacking. Here, we used high-speed amperometry with enzyme-based GLU and enzyme-free GLU-null biosensors to examine changes in extracellular GLU levels in the ventral tegmental area (VTA) and nucleus accumbens shell (NAcc) induced by intravenous nicotine in a low, behaviorally active dose (30 μg/kg) in freely moving rats. Using this approach, we found that the initial nicotine injection in drug-naive conditions induces rapid, transient, and relatively small GLU release (~ 90 nM; latency ~ 15 s, duration ~ 60 s) that is correlative in the VTA and NAcc. Following subsequent nicotine injections within the same session, this phasic GLU release was supplemented by stronger tonic increases in GLU levels (100-300 nM) that paralleled increases in drug-induced locomotor activation. GLU responses induced by repeated nicotine injections were more phasic and stronger in the NAcc than in VTA. Therefore, GLU is phasically released within the brain's reinforcement circuit following intravenous nicotine administration. Robust enhancement of nicotine-induced GLU responses following repeated injections suggests this change as an important mediator of sensitized behavioral and neural effects of nicotine. By using high-speed amperometry with glutamate (GLU) biosensors, we show that i.v. nicotine at a low, behaviorally relevant dose induces rapid GLU release in the NAcc and VTA that is enhanced following repeated drug injections. This is the first study reporting second-scale fluctuations in extracellular GLU levels induced by nicotine in two critical structures of the motivation-reinforcement circuit and rapid sensitization of GLU responses coupled with locomotor sensitization.
MeSH term(s)	Animals ; Biosensing Techniques ; Dose-Response Relationship, Drug ; Glutamine/metabolism ; Injections, Intravenous ; Locomotion/drug effects ; Male ; Nicotine/administration & dosage ; Nicotine/pharmacology ; Nucleus Accumbens/drug effects ; Nucleus Accumbens/metabolism ; Rats ; Rats, Long-Evans ; Ventral Tegmental Area/drug effects ; Ventral Tegmental Area/metabolism
Chemical Substances	Glutamine (0RH81L854J) ; Nicotine (6M3C89ZY6R)
Language	English
Publishing date	2013-10-21
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	80158-6
ISSN	1471-4159 ; 0022-3042 ; 1474-1644
ISSN (online)	1471-4159
ISSN	0022-3042 ; 1474-1644
DOI	10.1111/jnc.12450
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Article ; Online: The opioid receptors as targets for drug abuse medication.

Noble, Florence / Lenoir, Magalie / Marie, Nicolas

British journal of pharmacology

2015 Volume 172, Issue 16, Page(s) 3964–3979

Abstract: The endogenous opioid system is largely expressed in the brain, and both endogenous opioid peptides and receptors are present in areas associated with reward and motivation. It is well known that this endogenous system plays a key role in many aspects of ...

Abstract	The endogenous opioid system is largely expressed in the brain, and both endogenous opioid peptides and receptors are present in areas associated with reward and motivation. It is well known that this endogenous system plays a key role in many aspects of addictive behaviours. The present review summarizes the modifications of the opioid system induced by chronic treatment with drugs of abuse reported in preclinical and clinical studies, as well as the action of opioid antagonists and agonists on the reinforcing effects of drugs of abuse, with therapeutic perspectives. We have focused on the effects of chronic psychostimulants, alcohol and nicotine exposure. Taken together, the changes in both opioid peptides and opioid receptors in different brain structures following acute or chronic exposure to these drugs of abuse clearly identify the opioid system as a potential target for the development of effective pharmacotherapy for the treatment of addiction and the prevention of relapse.
MeSH term(s)	Alcohol Drinking/metabolism ; Animals ; Central Nervous System Stimulants/pharmacology ; Cocaine/pharmacology ; Ganglionic Stimulants/pharmacology ; Humans ; Nicotine/pharmacology ; Receptors, Opioid/metabolism ; Substance-Related Disorders/drug therapy ; Substance-Related Disorders/metabolism
Chemical Substances	Central Nervous System Stimulants ; Ganglionic Stimulants ; Receptors, Opioid ; Nicotine (6M3C89ZY6R) ; Cocaine (I5Y540LHVR)
Language	English
Publishing date	2015-08
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	80081-8
ISSN	1476-5381 ; 0007-1188
ISSN (online)	1476-5381
ISSN	0007-1188
DOI	10.1111/bph.13190
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Article ; Online: Rapid fluctuations in extracellular brain glucose levels induced by natural arousing stimuli and intravenous cocaine: fueling the brain during neural activation.

Kiyatkin, Eugene A / Lenoir, Magalie

Journal of neurophysiology

2012 Volume 108, Issue 6, Page(s) 1669–1684

Abstract: Glucose, a primary energetic substrate for neural activity, is continuously influenced by two opposing forces that tend to either decrease its extracellular levels due to enhanced utilization in neural cells or increase its levels due to entry from ... ...

Abstract	Glucose, a primary energetic substrate for neural activity, is continuously influenced by two opposing forces that tend to either decrease its extracellular levels due to enhanced utilization in neural cells or increase its levels due to entry from peripheral circulation via enhanced cerebral blood flow. How this balance is maintained under physiological conditions and changed during neural activation remains unclear. To clarify this issue, enzyme-based glucose sensors coupled with high-speed amperometry were used in freely moving rats to evaluate fluctuations in extracellular glucose levels induced by brief audio stimulus, tail pinch (TP), social interaction with another rat (SI), and intravenous cocaine (1 mg/kg). Measurements were performed in nucleus accumbens (NAcc) and substantia nigra pars reticulata (SNr), which drastically differ in neuronal activity. In NAcc, where most cells are powerfully excited after salient stimulation, glucose levels rapidly (latency 2-6 s) increased (30-70 μM or 6-14% over baseline) by all stimuli; the increase differed in magnitude and duration for each stimulus. In SNr, where most cells are transiently inhibited by salient stimuli, TP, SI, and cocaine induced a biphasic glucose response, with the initial decrease (-20-40 μM or 5-10% below baseline) followed by a reboundlike increase. The critical role of neuronal activity in mediating the initial glucose response was confirmed by monitoring glucose currents after local microinjections of glutamate (GLU) or procaine (PRO). While intra-NAcc injection of GLU transiently increased glucose levels in this structure, intra-SNr PRO injection resulted in rapid, transient decreases in SNr glucose. Therefore, extracellular glucose levels in the brain change very rapidly after physiological and pharmacological stimulation, the response is structure specific, and the pattern of neuronal activity appears to be a critical factor determining direction and magnitude of physiological fluctuations in glucose levels.
MeSH term(s)	Administration, Intravenous ; Animals ; Arousal/physiology ; Brain/metabolism ; Cocaine/administration & dosage ; Cocaine/pharmacology ; Extracellular Space/chemistry ; Extracellular Space/metabolism ; Glucose/analysis ; Glucose/metabolism ; Glutamic Acid/pharmacology ; Male ; Neurons/physiology ; Nucleus Accumbens/metabolism ; Nucleus Accumbens/physiology ; Procaine/pharmacology ; Rats ; Rats, Long-Evans ; Social Environment ; Substantia Nigra/metabolism ; Substantia Nigra/physiology ; Touch
Chemical Substances	Glutamic Acid (3KX376GY7L) ; Procaine (4Z8Y51M438) ; Cocaine (I5Y540LHVR) ; Glucose (IY9XDZ35W2)
Language	English
Publishing date	2012-06-20
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	80161-6
ISSN	1522-1598 ; 0022-3077
ISSN (online)	1522-1598
ISSN	0022-3077
DOI	10.1152/jn.00521.2012
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Article ; Online: Critical role of peripheral actions of intravenous nicotine in mediating its central effects.

Lenoir, Magalie / Kiyatkin, Eugene A

Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology

2011 Volume 36, Issue 10, Page(s) 2125–2138

Abstract: In addition to its direct action on central neurons, nicotine (NIC) activates multiple nicotinic acetylcholine receptors localized on afferent terminals of sensory nerves at the sites of its administration. Although the activation of these receptors is ... ...

Abstract	In addition to its direct action on central neurons, nicotine (NIC) activates multiple nicotinic acetylcholine receptors localized on afferent terminals of sensory nerves at the sites of its administration. Although the activation of these receptors is important in mediating the primary sensory and cardiovascular effects of NIC, their role in triggering and maintaining the neural effects of NIC remains unclear. Using high-speed electroencephalography (EEG) and electromyography (EMG) recordings in freely moving rats, we showed that NIC at low intravenous (i.v.) doses (10-30 μg/kg) induced rapid, strong, and prolonged EEG desynchronization both in the cortex and ventral tegmental area (with decreases in α and robust increases in β and γ frequencies) and neck EMG activation that began during the injection (∼5 s). EEG and EMG effects of NIC were drastically reduced by pre-treatment with hexamethonium, a peripherally acting NIC antagonist, and the immediate EEG effects of NIC were strongly inhibited during urethane anesthesia. Although NIC pyrrolidine methiodide, a quaternary NIC analog that cannot enter the brain, also induced rapid EEG desynchronization, its effects were much shorter and weaker than those of NIC. Therefore, NIC by acting on peripheral nicotinic receptors provides a major contribution to its rapid, excitatory effects following i.v. administration. Since this action creates a sensory signal that rapidly reaches the brain via neural pathways and precedes the slower and more prolonged direct actions of NIC on brain cells, it could have a major role in associative learning and changes in the behavioral and physiological effects of NIC following its repeated use.
MeSH term(s)	Animals ; Brain Chemistry/drug effects ; Brain Chemistry/physiology ; Electroencephalography/drug effects ; Electromyography/drug effects ; Electromyography/methods ; Injections, Intravenous ; Male ; Neural Pathways/drug effects ; Neural Pathways/metabolism ; Neural Pathways/physiology ; Nicotine/administration & dosage ; Nicotine/toxicity ; Peripheral Nerves/drug effects ; Peripheral Nerves/metabolism ; Peripheral Nerves/physiology ; Rats ; Rats, Long-Evans ; Receptors, Nicotinic/metabolism
Chemical Substances	Receptors, Nicotinic ; Nicotine (6M3C89ZY6R)
Language	English
Publishing date	2011-06-08
Publishing country	England
Document type	Comparative Study ; Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	639471-1
ISSN	1740-634X ; 0893-133X
ISSN (online)	1740-634X
ISSN	0893-133X
DOI	10.1038/npp.2011.104
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Article ; Online: Intravenous saline injection as an interoceptive signal in rats.

Kiyatkin, Eugene A / Lenoir, Magalie

Psychopharmacology

2011 Volume 217, Issue 3, Page(s) 387–396

Abstract: Rationale: Addictive drugs are commonly delivered in the organism by means of intravenous (i.v.) injections. Since saline mimics the blood environment by basic ionic properties and pH, it is generally assumed that it should not have any physiological ... ...

Abstract	Rationale: Addictive drugs are commonly delivered in the organism by means of intravenous (i.v.) injections. Since saline mimics the blood environment by basic ionic properties and pH, it is generally assumed that it should not have any physiological effects, serving as a control for the effects induced by drugs. Objective: The aim of the study was to examine central, behavioral, and physiological effects of stress- and cue-free i.v. saline injection in freely moving rats. Methods: We examined how a typical low-volume and slow-speed saline injections affect cortical electroencephalograpy (EEG), neck electromyography (EMG), locomotor activity as well as central and peripheral temperatures. Results: Saline injection made during slow-wave synchronized activity induces rapid transient EEG desynchronization, manifesting as a drop of EEG total power, decrease in alpha activity, and increases in beta and gamma activities. Saline injection did not affect locomotor activity as well as brain and body temperatures, but induced a transient increase in neck EMG activity and a rapid brief drop in skin temperature, suggesting peripheral vasoconstriction. These responses were virtually fully absent when saline injection was made during naturally occurring desynchronized EEG activity during behavioral activity. Conclusions: Since i.v. injection is able to produce a peripheral sensory signal that is transmitted rapidly to the CNS and followed by a more prolonged effect of the injected drug on brain cells, with repeated drug administrations, the injection itself could play a role of drug-related sensory cue, thus inducing conditioned physiological responses and altering the effects of injected drugs.
MeSH term(s)	Animals ; Body Temperature/drug effects ; Body Temperature/physiology ; Brain/drug effects ; Brain/physiology ; Cortical Synchronization ; Electroencephalography ; Electromyography ; Injections, Intravenous ; Male ; Motor Activity/drug effects ; Motor Activity/physiology ; Neck Muscles/drug effects ; Neck Muscles/innervation ; Neck Muscles/physiology ; Peripheral Nerves/drug effects ; Peripheral Nerves/physiology ; Rats ; Rats, Long-Evans ; Sodium Chloride/administration & dosage ; Sodium Chloride/pharmacology
Chemical Substances	Sodium Chloride (451W47IQ8X)
Language	English
Publishing date	2011-04-15
Publishing country	Germany
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	130601-7
ISSN	1432-2072 ; 0033-3158
ISSN (online)	1432-2072
ISSN	0033-3158
DOI	10.1007/s00213-011-2294-4
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