Adolescence is a time of considerable transformation in stress-sensitive brain regions that play key roles in the processing of rewarding and social/emotional stimuli and in areas that exert regulatory control over these regions. Given that lasting effects of substances are most likely to occur when systems sensitive to those substances are changing developmentally, we hypothesize that adolescent intermittent ethanol (AIE) exposure will induce lasting effects on social behavior and on the social rewarding and aversive effects of ethanol, leading to persistent elevations in adult intake due in part to alcohol's social anxiolytic properties. Indeed, social rewarding effects of alcohol are critical for the initiation of alcohol use in adolescence and escalation to heavy drinking among individuals with social anxiety, with socially anxious alcoholics showing greater levels of social impairment than non-dependent, socially anxious individuals. The proposed studies will investigate the consequences of voluntary and experimenter-administered adolescent intermittent alcohol (AIE) on later social anxiety and reward, the efficacy of alcohol for countering these lasting perturbations in social behavior, and the impact on later voluntary intake of ethanol, along with neural/genetic adaptations underlying these effects. Using synergisms provided by the NADIA, the proposed research will address the following aims: (1) test whether AIE increases baseline levels of anxiety-like behavior under social circumstances in adulthood and exacerbates stress-induced social anxiety, and determine the efficacy of acute ethanol for reversing this social anxiety;(2) determine whether AIE exposure disrupts the rewarding and/or hedonic value of social stimuli, whether these alterations are further exacerbated by stress, and the efficacy of acute ethanol for reversing these effects;(3) assess whether AIE enhances ethanol drinking in adulthood and decreases sensitivity to the aversive properties of ethanol, and whether these effects of AIE are further exacerbated by social context in adulthood;(4) investigate AIE effects on dopamine transmission during adulthood by measuring real-time dopamine release in nucleus accumbens in response to social stimuli and assessing dopamine-related gene expression in key limbic regions.

Public Health Relevance

The proposed investigations of lasting effects of adolescent alcohol exposure on social anxiety, alcohol's anxiolytic properties, and underiying neural/genetic adaptations are of considerable relevance, given the importance of alcohol's social rewarding properties in initiating use and escalating to heavy drinking among individuals with social anxiety, along with the greater social impairment seen in socially anxious alcoholics.

Agency
National Institute of Health (NIH)
Institute
National Institute on Alcohol Abuse and Alcoholism (NIAAA)
Type
Research Project--Cooperative Agreements (U01)
Project #
5U01AA019972-04
Application #
8531065
Study Section
Special Emphasis Panel (ZAA1-DD (11))
Program Officer
Bechtholt-Gompf, Anita
Project Start
2010-09-05
Project End
2015-08-31
Budget Start
2013-09-01
Budget End
2014-08-31
Support Year
4
Fiscal Year
2013
Total Cost
$313,257
Indirect Cost
$76,387
Name
State University of NY, Binghamton
Department
Psychology
Type
Schools of Arts and Sciences
DUNS #
090189965
City
Binghamton
State
NY
Country
United States
Zip Code
13902
Doremus-Fitzwater, Tamara L; Spear, Linda P (2016) Reward-centricity and attenuated aversions: An adolescent phenotype emerging from studies in laboratory animals. Neurosci Biobehav Rev 70:121-134
Shnitko, Tatiana A; Spear, Linda P; Robinson, Donita L (2016) Adolescent binge-like alcohol alters sensitivity to acute alcohol effects on dopamine release in the nucleus accumbens of adult rats. Psychopharmacology (Berl) 233:361-71
Spear, Linda Patia (2016) Consequences of adolescent use of alcohol and other drugs: Studies using rodent models. Neurosci Biobehav Rev 70:228-243
Varlinskaya, Elena I; Truxell, Eric M; Spear, Linda P (2015) Ethanol intake under social circumstances or alone in sprague-dawley rats: impact of age, sex, social activity, and social anxiety-like behavior. Alcohol Clin Exp Res 39:117-25
Varlinskaya, Elena I; Truxell, Eric M; Spear, Linda P (2015) Sex differences in sensitivity to the social consequences of acute ethanol and social drinking during adolescence. Behav Brain Res 282:6-13
Spear, Linda Patia (2015) Adolescent alcohol exposure: Are there separable vulnerable periods within adolescence? Physiol Behav 148:122-30
Varlinskaya, Elena I; Spear, Linda P (2015) Social consequences of ethanol: Impact of age, stress, and prior history of ethanol exposure. Physiol Behav 148:145-50
Saalfield, Jessica; Spear, Linda (2015) Consequences of repeated ethanol exposure during early or late adolescence on conditioned taste aversions in rats. Dev Cogn Neurosci 16:174-82
McClory, Alexander James; Spear, Linda Patia (2014) Effects of ethanol exposure during adolescence or in adulthood on Pavlovian conditioned approach in Sprague-Dawley rats. Alcohol 48:755-63
Shnitko, Tatiana A; Robinson, Donita L (2014) Anatomical and pharmacological characterization of catecholamine transients in the medial prefrontal cortex evoked by ventral tegmental area stimulation. Synapse 68:131-43

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