Social context induces two unique patterns of c-Fos expression in adolescent and adult rats.

The study assessed possible age differences in brain activation patterns to low dose ethanol (.5 g/kg intraperitoneally) and the influence of social context on this activation. Early adolescent or young adult male Sprague-Dawley rats were placed either alone or with an unfamiliar partner of the same age and sex following saline or ethanol administration. c-Fos protein immunoreactivity was used to index neuronal activation in 15 regions of interest. Ethanol had little effect on c-Fos activation. In adolescents, social context activated an "autonomic" network including the basolateral and central amygdala, bed nucleus of the stria terminalis, lateral hypothalamus, and lateral septum. In contrast, when adult rats were alone, activation was evident in a "reward" network that included the substantia nigra, nucleus accumbens, anterior cingulate and orbitofrontal cortices, lateral parabrachial nucleus, and locus coeruleus.

[1]  D. Gauvin,et al.  Aversive attributes of ethanol can be attenuated by dyadic social interaction in the rat. , 1994, Alcohol.

[2]  L. Spear,et al.  Effect of stress on the voluntary intake of a sweetened ethanol solution in pair-housed adolescent and adult rats. , 2005, Alcoholism, clinical and experimental research.

[3]  N. S. Pentkowski,et al.  Environmental living conditions introduced during forced abstinence alter cocaine-seeking behavior and Fos protein expression , 2010, Neuroscience.

[4]  A. R. Willey,et al.  Social interactions and 50kHz ultrasonic vocalizations in adolescent and adult rats , 2009, Behavioural Brain Research.

[5]  C. Scavone,et al.  Environmental modulation of ethanol-induced locomotor activity: Correlation with neuronal activity in distinct brain regions of adolescent and adult Swiss mice , 2008, Brain Research.

[6]  Y. Mori,et al.  Two types of social buffering differentially mitigate conditioned fear responses , 2007, The European journal of neuroscience.

[7]  L. Spear,et al.  Social interactions in adolescent and adult Sprague–Dawley rats: Impact of social deprivation and test context familiarity , 2008, Behavioural Brain Research.

[8]  R. Oades,et al.  Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity , 1987, Brain Research Reviews.

[9]  G. Wolterink,et al.  The effects of neonatal lesions in the amygdala or ventral hippocampus on social behaviour later in life , 2002, Behavioural Brain Research.

[10]  J. Rosenblatt,et al.  Induction of c‐Fos‐like and FosB‐like immunoreactivity reveals forebrain neuronal populations involved differentially in pup‐mediated maternal behavior in juvenile and adult rats , 2000, The Journal of comparative neurology.

[11]  J. Panksepp,et al.  In search of the neurobiological substrates for social playfulness in mammalian brains , 2011, Neuroscience & Biobehavioral Reviews.

[12]  Brent A. Vogt,et al.  CHAPTER 22 – Cingulate Cortex and Disease Models , 2004 .

[13]  L. Spear,et al.  Differences in the social consequences of ethanol emerge during the course of adolescence in rats: social facilitation, social inhibition, and anxiolysis. , 2006, Developmental psychobiology.

[14]  W. Hartup,et al.  Friendships and adaptation in the life course. , 1997 .

[15]  B. Jacobs,et al.  Single-unit response of noradrenergic neurons in the locus coeruleus of freely moving cats. II. Adaptation to chronically presented stressful stimuli , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  M. Schachner,et al.  Novelty-induced increased expression of immediate-early genes c-fos and arg 3.1 in the mouse brain. , 1999, Journal of neurobiology.

[17]  S. Kelly,et al.  Effects of alcohol exposure during development on play behavior and c-Fos expression in response to play behavior , 2008, Behavioural Brain Research.

[18]  R. Hitzemann,et al.  Genetics ethanol and the Fos response: a comparison of the C57BL/6J and DBA/2J inbred mouse strains. , 1997, Alcoholism, clinical and experimental research.

[19]  S. Blakemore The social brain in adolescence , 2008, Nature Reviews Neuroscience.

[20]  Sylvia Kaiser,et al.  Social buffering of the stress response: Diversity, mechanisms, and functions , 2009, Frontiers in Neuroendocrinology.

[21]  S. Foote Chapter IV The primate locus coeruleus: the chemical neuroanatomy of the nucleus, its efferent projections, and its target receptors , 1997 .

[22]  M Tanaka,et al.  Noradrenaline systems in the hypothalamus, amygdala and locus coeruleus are involved in the provocation of anxiety: basic studies. , 2000, European journal of pharmacology.

[23]  L. Spear,et al.  Novel-object place conditioning in adolescent and adult male and female rats: effects of social isolation , 2003, Physiology & Behavior.

[24]  Sulie L. Chang,et al.  Activation and desensitization of Fos immunoreactivity in the rat brain following ethanol administration , 1995, Brain Research.

[25]  L. Spear,et al.  Acute effects of ethanol on social behavior of adolescent and adult rats: role of familiarity of the test situation. , 2002, Alcoholism, clinical and experimental research.

[26]  F. Cirulli,et al.  Behavioral and hormonal effects of partner familiarity in periadolescent rat pairs upon novelty exposure , 1999, Psychoneuroendocrinology.

[27]  F. Crews,et al.  Regional specificity of ethanol and NMDA action in brain revealed with FOS-like immunohistochemistry and differential routes of drug administration. , 2001, Alcoholism, clinical and experimental research.

[28]  T. Palfai,et al.  Examining the role of drinking motives in college student alcohol use and problems. , 2003, Psychology of addictive behaviors : journal of the Society of Psychologists in Addictive Behaviors.

[29]  James P. Lister,et al.  Prenatal Protein Malnutrition in Rats Alters the c-Fos Response of Neurons in the Anterior Cingulate and Medial Prefrontal Region to Behavioral Stress , 2004, Nutritional neuroscience.

[30]  M. Morales,et al.  Acute ethanol induction of c-Fos immunoreactivity in pre-pro-enkephalin expressing neurons of the central nucleus of the amygdala , 2000, Brain Research.

[31]  L. Spear,et al.  Sex Differences in Ethanol Intake and Sensitivity to Aversive Effects during Adolescence and Adulthood , 2009, Alcohol and alcoholism.

[32]  L. Vanderschuren,et al.  The neurobiology of social play behavior in rats , 1997, Neuroscience & Biobehavioral Reviews.

[33]  D. Wirtshafter Cholinergic involvement in the cortical and hippocampal Fos expression induced in the rat by placement in a novel environment , 2005, Brain Research.

[34]  A. A. Alcantara,et al.  Ethanol-induced Fos immunoreactivity in the extended amygdala and hypothalamus of the rat brain: focus on cholinergic interneurons of the nucleus accumbens. , 2004, Alcoholism, clinical and experimental research.

[35]  J. Herman,et al.  Neural regulation of endocrine and autonomic stress responses , 2009, Nature Reviews Neuroscience.

[36]  Duane T. Wegener,et al.  Evaluating the use of exploratory factor analysis in psychological research. , 1999 .

[37]  G. Awatramani,et al.  Adolescent development alters stressor-induced Fos immunoreactivity in rat brain , 1998, Neuroscience.

[38]  L. Spear,et al.  Time course of elevated ethanol intake in adolescent relative to adult rats under continuous, voluntary-access conditions. , 2007, Alcoholism, clinical and experimental research.

[39]  Kathrin Cohen Kadosh,et al.  The social brain in adolescence: Evidence from functional magnetic resonance imaging and behavioural studies , 2011, Neuroscience & Biobehavioral Reviews.

[40]  J. Canales Catalase-independent early-gene expression in rat brain following acute ethanol exposure , 2004, Brain Research.

[41]  T. Kikusui,et al.  Partner's stress status influences social buffering effects in rats. , 2004, Behavioral neuroscience.

[42]  Activation of Fos-like immunoreactivity in the medial preoptic area and limbic structures by maternal and social interactions in rats. , 1994, Behavioral neuroscience.

[43]  S. Maier,et al.  Inescapable but not escapable stress leads to increased struggling behavior and basolateral amygdala c-fos gene expression in response to subsequent novel stress challenge , 2010, Neuroscience.

[44]  M. Naassila,et al.  Ethanol-sensitive brain regions in rat and mouse: a cartographic review, using immediate early gene expression. , 2009, Alcoholism, clinical and experimental research.

[45]  Nakia S. Gordon,et al.  Expression of c-fos gene activation during rough and tumble play in juvenile rats , 2002, Brain Research Bulletin.

[46]  C. McCormick,et al.  Locomotor activity to nicotine and Fos immunoreactivity in the paraventricular nucleus of the hypothalamus in adolescent socially-stressed rats , 2007, Pharmacology Biochemistry and Behavior.

[47]  L. Spear,et al.  Rewarding properties of social interactions in adolescent and adult male and female rats: impact of social versus isolate housing of subjects and partners. , 2004, Developmental psychobiology.

[48]  K. Beck,et al.  The relationship of social context of drinking, perceived social norms, and parental influence to various drinking patterns of adolescents. , 1996, Addictive behaviors.

[49]  F. Bloom,et al.  Differential sensitivity of c-Fos expression in hippocampus and other brain regions to moderate and low doses of alcohol , 1997, Molecular Psychiatry.

[50]  T. Curran,et al.  Expression of c-fos protein in brain: metabolic mapping at the cellular level. , 1988, Science.

[51]  J. Panksepp,et al.  Dorsomedial diencephalic involvement in the juvenile play of rats. , 1985, Behavioral neuroscience.

[52]  T. Dinan,et al.  Restraint stress-induced brain activation patterns in two strains of mice differing in their anxiety behaviour , 2010, Behavioural Brain Research.

[53]  A. Oliverio,et al.  Distinct patterns of Fos immunoreactivity in striatum and hippocampus induced by different kinds of novelty in mice , 2010, Neurobiology of Learning and Memory.

[54]  A. Lawrence,et al.  Chronic cold stress regulates ascending noradrenergic pathways , 2004, Neuroscience.

[55]  Jaak Panksepp,et al.  The psychobiology of play: Theoretical and methodological perspectives , 1984, Neuroscience & Biobehavioral Reviews.

[56]  L. Steinberg,et al.  Peers increase adolescent risk taking by enhancing activity in the brain's reward circuitry. , 2011, Developmental science.

[57]  E. M. Scordalakes,et al.  Social interaction with an intoxicated sibling can result in increased intake of ethanol by periadolescent rats. , 2001, Developmental psychobiology.

[58]  B. Pearce,et al.  Principles and pitfalls in the analysis of prenatal treatment effects in multiparous species. , 1992, Neurotoxicology and teratology.

[59]  A. Kelley,et al.  Food-associated cues alter forebrain functional connectivity as assessed with immediate early gene and proenkephalin expression , 2007, BMC Biology.