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Article: Chronic alcohol consumption alters sex-dependent BNST neuron function in rhesus macaques.

Pleil, Kristen E / Grant, Kathleen A / Cuzon Carlson, Verginia C / Kash, Thomas L

2024 Volume 31, Page(s) 100638

Abstract: Repeated alcohol drinking contributes to a number of neuropsychiatric diseases, including alcohol use disorder and co-expressed anxiety and mood disorders. Women are more susceptible to the development and expression of these diseases with the same ... ...

Abstract	Repeated alcohol drinking contributes to a number of neuropsychiatric diseases, including alcohol use disorder and co-expressed anxiety and mood disorders. Women are more susceptible to the development and expression of these diseases with the same history of alcohol exposure as men, suggesting they may be more sensitive to alcohol-induced plasticity in limbic brain regions controlling alcohol drinking, stress responsivity, and reward processing, among other behaviors. Using a translational model of alcohol drinking in rhesus monkeys, we examined sex differences in the basal function and plasticity of neurons in the bed nucleus of the stria terminalis (BNST), a brain region in the extended amygdala shown to be a hub circuit node dysregulated in individuals with anxiety and alcohol use disorder. We performed slice electrophysiology recordings from BNST neurons in male and female monkeys following daily "open access" (22 h/day) to 4% ethanol and water for more than one year or control conditions. We found that BNST neurons from control females had reduced overall current density, hyperpolarization-activated depolarizing current (I
Language	English
Publishing date	2024-04-30
Publishing country	United States
Document type	Journal Article
ZDB-ID	2816500-7
ISSN	2352-2895
ISSN	2352-2895
DOI	10.1016/j.ynstr.2024.100638
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Article: GABA and Glutamate Synaptic Coadaptations to Chronic Ethanol in the Striatum.

Cuzon Carlson, Verginia C

Handbook of experimental pharmacology

2018 Volume 248, Page(s) 79–112

Abstract: Alcohol (ethanol) is a widely used and abused drug with approximately 90% of adults over the age of 18 consuming alcohol at some point in their lifetime. Alcohol exerts its actions through multiple neurotransmitter systems within the brain, most notably ... ...

Abstract	Alcohol (ethanol) is a widely used and abused drug with approximately 90% of adults over the age of 18 consuming alcohol at some point in their lifetime. Alcohol exerts its actions through multiple neurotransmitter systems within the brain, most notably the GABAergic and glutamatergic systems. Alcohol's actions on GABAergic and glutamatergic neurotransmission have been suggested to underlie the acute behavioral effects of ethanol. The striatum is the primary input nucleus of the basal ganglia that plays a role in motor and reward systems. The effect of ethanol on GABAergic and glutamatergic neurotransmission within striatal circuitry has been thought to underlie ethanol taking, seeking, withdrawal and relapse. This chapter reviews the effects of ethanol on GABAergic and glutamatergic transmission, highlighting the dynamic changes in striatal circuitry from acute to chronic exposure and withdrawal.
MeSH term(s)	Corpus Striatum/drug effects ; Ethanol/pharmacology ; Glutamic Acid/physiology ; Humans ; Reward ; Synaptic Transmission ; gamma-Aminobutyric Acid/physiology
Chemical Substances	Ethanol (3K9958V90M) ; Glutamic Acid (3KX376GY7L) ; gamma-Aminobutyric Acid (56-12-2)
Language	English
Publishing date	2018-02-19
Publishing country	Germany
Document type	Journal Article
ISSN	0171-2004
ISSN	0171-2004
DOI	10.1007/164_2018_98
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Article ; Online: Impact of putamen inhibition by DREADDs on schedule-induced drinking in rhesus monkeys.

Grant, Kathleen A / Newman, Natali N / Gonzales, Steven W / Cuzon Carlson, Verginia C

Journal of the experimental analysis of behavior

2022 Volume 117, Issue 3, Page(s) 493–504

Abstract: The putamen is a nucleus within the sensory-motor striatal network that is involved in automatic, habitual actions. Schedule-induced polydipsia (SIP) is highly automated behavior, reliably occurring under intermediate interval schedules of reinforcement. ...

Abstract	The putamen is a nucleus within the sensory-motor striatal network that is involved in automatic, habitual actions. Schedule-induced polydipsia (SIP) is highly automated behavior, reliably occurring under intermediate interval schedules of reinforcement. The effect of putamen inhibition in mediating SIP of water and ethanol (4% w/v) under a Fixed Time 5-min (FT-5 min) schedule for food delivery was tested in 12 rhesus monkeys (6 male, 6 female). Water and ethanol SIP sessions ended after set volumes were consumed. Baseline patterns of SIP intake differed between water and ethanol SIP in volume but not in pattern of drinking. Activation of the designer receptor exclusively activated by designer drug (DREADD: hM4Di) with deschloroclozapine (DCZ; 300 μg/kg, i.m.) administered 30 min prior to the onset of the SIP session, for four consecutive sessions. DCZ administration increased the postpellet drink volume and reduced the time to drink both water and ethanol. Although the effect of DCZ treatment was similar for increasing SIP with either water or ethanol, post-DCZ return to baseline SIP rates of differed, perhaps highlighting the effect of a state dependency with ethanol SIP. Overall, the study shows that targeting the putamen with the inhibitory DREADD produces a reversible, reproducible and reliable increase in adjunctive drinking.
MeSH term(s)	Animals ; Drinking Behavior ; Ethanol/pharmacology ; Female ; Macaca mulatta ; Male ; Putamen ; Reinforcement Schedule ; Water
Chemical Substances	Water (059QF0KO0R) ; Ethanol (3K9958V90M)
Language	English
Publishing date	2022-04-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	219405-3
ISSN	1938-3711 ; 0022-5002
ISSN (online)	1938-3711
ISSN	0022-5002
DOI	10.1002/jeab.761
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Article: Synchrony between midbrain gene transcription and dopamine terminal regulation is modulated by chronic alcohol drinking.

Farahbakhsh, Zahra Z / Holleran, Katherine M / Sens, Jonathon P / Fordahl, Steve C / Mauterer, Madelyn I / López, Alberto J / Cuzon Carlson, Verginia C / Kiraly, Drew D / Grant, Kathleen A / Jones, Sara R / Siciliano, Cody A

bioRxiv : the preprint server for biology

2024

Abstract: Alcohol use disorder is marked by disrupted behavioral and emotional states which persist into abstinence. The enduring synaptic alterations that remain despite the absence of alcohol are of interest for interventions to prevent relapse. Here, 28 male ... ...

Abstract	Alcohol use disorder is marked by disrupted behavioral and emotional states which persist into abstinence. The enduring synaptic alterations that remain despite the absence of alcohol are of interest for interventions to prevent relapse. Here, 28 male rhesus macaques underwent over 20 months of alcohol drinking interspersed with three 30-day forced abstinence periods. After the last abstinence period, we paired direct sub-second dopamine monitoring via
Language	English
Publishing date	2024-03-17
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.03.15.584711
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Article ; Online: Gestational alcohol exposure disrupts cognitive function and striatal circuits in adult offspring.

Cuzon Carlson, Verginia C / Gremel, Christina M / Lovinger, David M

Nature communications

2020 Volume 11, Issue 1, Page(s) 2555

Abstract: Fetal alcohol exposure (FAE) is the leading preventable developmental cause of cognitive dysfunction. Even in the absence of binge drinking, alcohol consumption during pregnancy can leave offspring deficient. However, the mechanisms underlying these ... ...

Abstract	Fetal alcohol exposure (FAE) is the leading preventable developmental cause of cognitive dysfunction. Even in the absence of binge drinking, alcohol consumption during pregnancy can leave offspring deficient. However, the mechanisms underlying these deficiencies are unknown. Using a mouse model of gestational ethanol exposure (GEE), we show increased instrumental lever-pressing and disruption of efficient habitual actions in adults, indicative of disrupted cognitive function. In vivo electrophysiology reveals disrupted action encoding in dorsolateral striatum (DLS) associated with altered habit learning. GEE mice exhibit decreased GABAergic transmission onto DLS projection neurons, including inputs from parvalbumin interneurons, and increased endocannabinoid tone. Chemogenetic activation of DLS parvalbumin interneurons reduces the elevated lever pressing of GEE mice. Pharmacologically increasing endocannabinoid tone mimics GEE effects on cognition and synaptic transmission. These findings show GEE induces long-lasting deficits in cognitive function that may contribute to human FAE, and identify potential mechanisms for future therapeutic targeting.
MeSH term(s)	Animals ; Cognition/drug effects ; Corpus Striatum/metabolism ; Corpus Striatum/physiology ; Corpus Striatum/physiopathology ; Ethanol/adverse effects ; Ethanol/metabolism ; Female ; Fetal Development ; Humans ; Male ; Maternal Exposure/adverse effects ; Mice, Inbred C57BL ; Pedigree ; Pregnancy ; Prenatal Exposure Delayed Effects/etiology ; Prenatal Exposure Delayed Effects/physiopathology ; Prenatal Exposure Delayed Effects/psychology
Chemical Substances	Ethanol (3K9958V90M)
Language	English
Publishing date	2020-05-22
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, N.I.H., Intramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-020-16385-4
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Article ; Online: Brain Functional Connectivity Mapping of Behavioral Flexibility in Rhesus Monkeys.

Grant, Kathleen A / Newman, Natali / Lynn, Colton / Davenport, Conor / Gonzales, Steven / Cuzon Carlson, Verginia C / Kroenke, Christopher D

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

2022 Volume 42, Issue 24, Page(s) 4867–4878

Abstract: The predisposition to engage in autonomous habitual behaviors has been associated with behavioral disorders, such as obsessive-compulsive disorder and addiction. Attentional set-shifting tasks (ASSTs), which incorporate changes governing the association ... ...

Abstract	The predisposition to engage in autonomous habitual behaviors has been associated with behavioral disorders, such as obsessive-compulsive disorder and addiction. Attentional set-shifting tasks (ASSTs), which incorporate changes governing the association of discriminative stimuli with contingent reinforcement, are commonly used to measure underlying processes of cognitive/behavioral flexibility. The purpose of this study was to identify primate brain networks that mediate trait-like deficits in ASST performance using resting-state fMRI. A self-pacing ASST was administered to three cohorts of rhesus monkeys (total
MeSH term(s)	Animals ; Brain/diagnostic imaging ; Brain Mapping/methods ; Female ; Lipopolysaccharides ; Macaca mulatta ; Magnetic Resonance Imaging/methods ; Male ; Neural Pathways
Chemical Substances	Lipopolysaccharides
Language	English
Publishing date	2022-05-12
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; 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.0816-21.2022
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Article ; Online: Neurobeachin, a promising target for use in the treatment of alcohol use disorder.

Cuzon Carlson, Verginia C / Aylwin, Carlos F / Carlson, Timothy L / Ford, Matthew / Mesnaoui, Houda / Lomniczi, Alejandro / Ferguson, Betsy / Cervera-Juanes, Rita P

Addiction biology

2021 Volume 27, Issue 1, Page(s) e13107

Abstract: Hazardous, heavy drinking increases risk for developing alcohol use disorder (AUD), which affects ~7% of adult Americans. Thus, understanding the molecular mechanisms promoting risk for heavy drinking is essential to developing more effective AUD ... ...

Abstract	Hazardous, heavy drinking increases risk for developing alcohol use disorder (AUD), which affects ~7% of adult Americans. Thus, understanding the molecular mechanisms promoting risk for heavy drinking is essential to developing more effective AUD pharmacotherapies than those currently approved by the FDA. Using genome-wide bisulfate sequencing, we identified DNA methylation (DNAm) signals within the nucleus accumbens core (NAcC) that differentiate nonheavy and heavy ethanol-drinking rhesus macaques. One differentially DNAm region (D-DMR) located within the gene neurobeachin (NBEA), which promotes synaptic membrane protein trafficking, was hypermethylated in heavy drinking macaques. A parallel study identified a similar NBEA D-DMR in human NAcC that distinguished alcoholic and nonalcoholic individuals. To investigate the role of NBEA in heavy ethanol drinking, we engineered a viral vector carrying a short hairpin RNA (shRNA) to reduce the expression of NBEA. Using two murine models of ethanol consumption: 4 days of drinking-in-the-dark and 4 weeks of chronic intermittent access, the knockdown of NBEA expression did not alter average ethanol consumption in either model. However, it did lead to a significant increase in the ethanol preference ratio. Following withdrawal, whole-cell patch clamp electrophysiological experiments revealed that Nbea knockdown led to an increase in spontaneous excitatory postsynaptic current amplitude with no alteration in spontaneous inhibitory postsynaptic currents, suggesting a specific role of NBEA in trafficking of glutamatergic receptors. Together, our findings suggest that NBEA could be targeted to modulate the preference for alcohol use.
MeSH term(s)	Adult ; Aged ; Alcohol Drinking/genetics ; Alcoholism/genetics ; Animals ; Carrier Proteins/genetics ; DNA Methylation/drug effects ; Humans ; Macaca mulatta ; Male ; Mice ; Mice, Inbred C57BL ; Middle Aged ; Nerve Tissue Proteins/genetics ; Nucleus Accumbens/drug effects
Chemical Substances	Carrier Proteins ; NBEA protein, human ; Nerve Tissue Proteins
Language	English
Publishing date	2021-10-26
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.13107
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Article ; Online: Characterization of DREADD receptor expression and function in rhesus macaques trained to discriminate ethanol.

Allen, Daicia C / Jimenez, Vanessa A / Carlson, Timothy L / Walter, Nicole A / Grant, Kathleen A / Cuzon Carlson, Verginia C

Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology

2021 Volume 47, Issue 4, Page(s) 857–865

Abstract: Circuit manipulation has been a staple technique in neuroscience to identify how the brain functions to control complex behaviors. Chemogenetics, including designer receptors exclusively activated by designer drugs (DREADDs), have proven to be a powerful ...

Abstract	Circuit manipulation has been a staple technique in neuroscience to identify how the brain functions to control complex behaviors. Chemogenetics, including designer receptors exclusively activated by designer drugs (DREADDs), have proven to be a powerful tool for the reversible modulation of discrete brain circuitry without the need for implantable devices, thereby making them especially useful in awake and unrestrained animals. This study used a DREADD approach to query the role of the nucleus accumbens (NAc) in mediating the interoceptive effects of 1.0 g/kg ethanol (i.g.) in rhesus monkeys (n = 7) using a drug discrimination procedure. After training, stereotaxic surgery was performed to introduce an AAV carrying the human muscarinic 4 receptor DREADD (hM4Di) bilaterally into the NAc. The hypothesis was that decreasing the output of the NAc by activation of hM4Di with the DREADD actuator, clozapine-n-oxide (CNO), would potentiate the discriminative stimulus effect of ethanol (i.e., a leftward shift the ethanol dose discrimination curve). The results showed individual variability shifts of the ethanol dose-response determination under DREADD activation. Characterization of the expression and function of hM4Di with MRI, immunohistochemical, and electrophysiological techniques found the selectivity of NAc transduction was proportional to behavioral effect. Specifically, the proportion of hM4Di expression restricted to the NAc was associated with the potency of the discriminative stimulus effects of ethanol. Together, these experiments highlight the NAc in mediating the interoceptive effects of ethanol, provide a framework for validation of chemogenetic tools in primates, and underscore the importance of robust within-subjects examination of DREADD expression for interpretation of behavioral findings.
MeSH term(s)	Animals ; Brain ; Clozapine/pharmacology ; Ethanol/pharmacology ; Macaca mulatta ; Nucleus Accumbens
Chemical Substances	Ethanol (3K9958V90M) ; Clozapine (J60AR2IKIC)
Language	English
Publishing date	2021-10-15
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	639471-1
ISSN	1740-634X ; 0893-133X
ISSN (online)	1740-634X
ISSN	0893-133X
DOI	10.1038/s41386-021-01181-5
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Article: Recurrent activity within microcircuits of macaque dorsolateral prefrontal cortex tracks cognitive flexibility.

Nolan, Suzanne O / Melugin, Patrick R / Erickson, Kirsty R / Adams, Wilson R / Farahbakhsh, Zahra Z / Mcgonigle, Colleen E / Kwon, Michelle H / Costa, Vincent D / Lapish, Christopher C / Hackett, Troy A / Cuzon Carlson, Verginia C / Constantinidis, Christos / Grant, Kathleen A / Siciliano, Cody A

bioRxiv : the preprint server for biology

2023

Abstract: Human and non-human primate data clearly implicate the dorsolateral prefrontal cortex (dlPFC) as critical for advanced cognitive ... ...

Abstract	Human and non-human primate data clearly implicate the dorsolateral prefrontal cortex (dlPFC) as critical for advanced cognitive functions
Language	English
Publishing date	2023-09-24
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.09.23.559125
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Article ; Online: Synaptic adaptations to chronic ethanol intake in male rhesus monkey dorsal striatum depend on age of drinking onset.

Cuzon Carlson, Verginia C / Grant, Kathleen A / Lovinger, David M

Neuropharmacology

2017 Volume 131, Page(s) 128–142

Abstract: One in 12 adults suffer with alcohol use disorder (AUD). Studies suggest the younger the age in which alcohol consumption begins the higher the probability of being diagnosed with AUD. Binge/excessive alcohol drinking involves a transition from flexible ... ...

Abstract	One in 12 adults suffer with alcohol use disorder (AUD). Studies suggest the younger the age in which alcohol consumption begins the higher the probability of being diagnosed with AUD. Binge/excessive alcohol drinking involves a transition from flexible to inflexible behavior likely involving the dorsal striatum (caudate and putamen nuclei). A major focus of this study was to examine the effect of age of drinking onset on subsequent chronic, voluntary ethanol intake and dorsal striatal circuitry. Data from rhesus monkeys (n = 45) that started drinking as adolescents, young adults or mature adults confirms an age-related risk for heavy drinking. Striatal neuroadaptations were examined using whole-cell patch clamp electrophysiology to record AMPA receptor-mediated miniature excitatory postsynaptic currents (mEPSCs) and GABA
MeSH term(s)	Adaptation, Physiological/drug effects ; Adaptation, Physiological/physiology ; Age Factors ; Age of Onset ; Alcohol Drinking/pathology ; Animals ; Central Nervous System Depressants/administration & dosage ; Central Nervous System Depressants/toxicity ; Corpus Striatum/pathology ; Corpus Striatum/physiopathology ; Disease Models, Animal ; Electric Stimulation ; Ethanol/administration & dosage ; Ethanol/toxicity ; Macaca mulatta ; Male ; Patch-Clamp Techniques ; Principal Component Analysis ; Self Administration ; Synapses/drug effects ; Synapses/physiology ; Synaptic Transmission/drug effects ; Synaptic Transmission/physiology ; gamma-Aminobutyric Acid/metabolism ; gamma-Aminobutyric Acid/pharmacology
Chemical Substances	Central Nervous System Depressants ; Ethanol (3K9958V90M) ; gamma-Aminobutyric Acid (56-12-2)
Language	English
Publishing date	2017-12-12
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, N.I.H., Intramural
ZDB-ID	218272-5
ISSN	1873-7064 ; 0028-3908
ISSN (online)	1873-7064
ISSN	0028-3908
DOI	10.1016/j.neuropharm.2017.12.010
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