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The International Journal on the Biology of Stress
Volume 26, 2023 - Issue 1
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Research Article

Voluntary alcohol consumption during distinct phases of adolescence differentially alters adult fear acquisition, extinction and renewal in male and female rats

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Article: 2278315 | Received 17 Jul 2023, Accepted 25 Oct 2023, Published online: 05 Nov 2023

References

  • Amodeo, L. R., Wills, D. N., Sanchez-Alavez, M., Nguyen, W., Conti, B., & Ehlers, C. L. (2018). Intermittent voluntary ethanol consumption combined with ethanol vapor exposure during adolescence increases drinking and alters other behaviors in adulthood in female and male rats. Alcohol, 73, 1–15. https://doi.org/10.1016/j.alcohol.2018.04.003
  • Bardo, M. T., Donohew, R. L., & Harrington, N. G. (1996). Psychobiology of novelty seeking and drug seeking behavior. Behavioural Brain Research, 77(1-2), 23–43. https://doi.org/10.1016/0166-4328(95)00203-0
  • Bava, S., & Tapert, S. F. (2010). Adolescent brain development and the risk for alcohol and other drug problems. Neuropsychology Review, 20(4), 398–413. https://doi.org/10.1007/s11065-010-9146-6
  • Bercum, F. M., Gomez, M. J. N., & Saddoris, M. P. (2023). Prefrontal cortex neurons in adult rats exposed to early life stress fail to appropriately signal the consequences of motivated actions. Physiology & Behavior, 263, 114107. https://doi.org/10.1016/j.physbeh.2023.114107
  • Bercum, F. M., Navarro Gomez, M. J., & Saddoris, M. P. (2021). Elevated fear responses to threatening cues in rats with early life stress is associated with greater excitability and loss of gamma oscillations in ventral-medial prefrontal cortex. Neurobiology of Learning and Memory, 185, 107541. https://doi.org/10.1016/j.nlm.2021.107541
  • Binette, A. N., Totty, M. S., & Maren, S. (2022). Sex differences in the immediate extinction deficit and renewal of extinguished fear in rats. PLoS One, 17(6), e0264797. https://doi.org/10.1371/journal.pone.0264797
  • Boutros, N., Semenova, S., Liu, W., Crews, F. T., & Markou, A. (2014). Adolescent intermittent ethanol exposure is associated with increased risky choice and decreased dopaminergic and cholinergic neuron markers in adult rats. The International Journal of Neuropsychopharmacology, 18(2), pyu003. https://doi.org/10.1093/ijnp/pyu003
  • Bouton, M. E., Maren, S., & McNally, G. P. (2021). Behavioral and neurobiological mechanisms of Pavlovian and extinction learning. Physiological Reviews, 101(2), 611–681. https://doi.org/10.1152/physrev.00016.2020
  • Brenhouse, H. C., & Andersen, S. L. (2011). Developmental trajectories during adolescence in males and females: a cross-species understanding of underlying brain changes. Neuroscience and Biobehavioral Reviews, 35(8), 1687–1703. https://doi.org/10.1016/j.neubiorev.2011.04.013
  • Broadwater, M., & Spear, L. P. (2013). Consequences of ethanol exposure on cued and contextual fear conditioning and extinction differ depending on timing of exposure during adolescence or adulthood. Behavioural Brain Research, 256, 10–19. https://doi.org/10.1016/j.bbr.2013.08.013
  • Broadwater, M. A., Lee, S.-H., Yu, Y., Zhu, H., Crews, F. T., Robinson, D. L., & Shih, Y.-Y. I. (2018). Adolescent alcohol exposure decreases frontostriatal resting-state functional connectivity in adulthood. Addiction Biology, 23(2), 810–823. https://doi.org/10.1111/adb.12530
  • Caballero, A., Flores-Barrera, E., Thomases, D. R., & Tseng, K. Y. (2020). Downregulation of parvalbumin expression in the prefrontal cortex during adolescence causes enduring prefrontal disinhibition in adulthood. Neuropsychopharmacology, 45(9), 1527–1535. https://doi.org/10.1038/s41386-020-0709-9
  • Conrod, P. J. (2016). Personality-targeted interventions for substance use and misuse. Current Addiction Reports, 3(4), 426–436. https://doi.org/10.1007/s40429-016-0127-6
  • Cooper, M. A., Grizzell, J. A., Whitten, C. J., & Burghardt, G. M. (2023). Comparing the ontogeny, neurobiology, and function of social play in hamsters and rats. Neuroscience and Biobehavioral Reviews, 147, 105102. https://doi.org/10.1016/j.neubiorev.2023.105102
  • Crews, F., He, J., & Hodge, C. (2007). Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacology, Biochemistry, and Behavior, 86(2), 189–199. https://doi.org/10.1016/j.pbb.2006.12.001
  • Dannenhoffer, C. A., Gómez-A, A., Macht, V. A., Jawad, R., Sutherland, E. B., Vetreno, R. P., Crews, F. T., Boettiger, C. A., & Robinson, D. L. (2022). Impact of adolescent intermittent ethanol exposure on interneurons and their surrounding perineuronal nets in adulthood. Alcoholism, Clinical and Experimental Research, 46(5), 759–769. https://doi.org/10.1111/acer.14810
  • DeGroot, S. R., Zhao-Shea, R., Chung, L., Klenowski, P. M., Sun, F., Molas, S., Gardner, P. D., Li, Y., & Tapper, A. R. (2020). Midbrain dopamine controls anxiety-like behavior by engaging unique interpeduncular nucleus microcircuitry. Biological Psychiatry, 88(11), 855–866. https://doi.org/10.1016/j.biopsych.2020.06.018
  • Desikan, A., Wills, D. N., & Ehlers, C. L. (2014). Ontogeny and adolescent alcohol exposure in Wistar rats: open field conflict, light/dark box and forced swim test. Pharmacology, Biochemistry, and Behavior, 122, 279–285. https://doi.org/10.1016/j.pbb.2014.04.011
  • Dorn, L. D. (2006). Measuring puberty. The Journal of Adolescent Health, 39(5), 625–626. https://doi.org/10.1016/j.jadohealth.2006.05.014
  • Fisher, H., Bright, N., Gallo, M., Pajser, A., & Pickens, C. L. (2017). Relationship of low doses of alcohol voluntarily consumed during adolescence and early adulthood with subsequent behavioral flexibility. Behavioural Pharmacology, 28(7), 531–544. https://doi.org/10.1097/FBP.0000000000000331
  • Flagel, S. B., Clark, J. J., Robinson, T. E., Mayo, L., Czuj, A., Willuhn, I., Akers, C. A., Clinton, S. M., Phillips, P. E. M., & Akil, H. (2011). A selective role for dopamine in stimulus-reward learning. Nature, 469(7328), 53–57. https://doi.org/10.1038/nature09588
  • Flagel, S. B., Waselus, M., Clinton, S. M., Watson, S. J., & Akil, H. (2014). Antecedents and consequences of drug abuse in rats selectively bred for high and low response to novelty. Neuropharmacology, 76 (Pt B), 425–436. https://doi.org/10.1016/j.neuropharm.2013.04.033
  • Fuhrmann, D., Knoll, L. J., & Blakemore, S.-J. (2015). Adolescence as a sensitive period of brain development. Trends in Cognitive Sciences, 19(10), 558–566. https://doi.org/10.1016/j.tics.2015.07.008
  • Garfinkel, S. N., Abelson, J. L., King, A. P., Sripada, R. K., Wang, X., Gaines, L. M., & Liberzon, I. (2014). Impaired contextual modulation of memories in PTSD: An fMRI and psychophysiological study of extinction retention and fear renewal. The Journal of Neuroscience, 34(40), 13435–13443. https://doi.org/10.1523/JNEUROSCI.4287-13.2014
  • Gass, J. T., Glen, W. B., McGonigal, J. T., Trantham-Davidson, H., Lopez, M. F., Randall, P. K., Yaxley, R., Floresco, S. B., & Chandler, L. J. (2014). Adolescent alcohol exposure reduces behavioral flexibility, promotes disinhibition, and increases resistance to extinction of ethanol self-administration in adulthood. Neuropsychopharmacology, 39(11), 2570–2583. https://doi.org/10.1038/npp.2014.109
  • Gilmore, J. H., Knickmeyer, R. C., & Gao, W. (2018). Imaging structural and functional brain development in early childhood. Nature Reviews. Neuroscience, 19(3), 123–137. https://doi.org/10.1038/nrn.2018.1
  • Grant, B. F., & Harford, T. C. (1995). Comorbidity between DSM-IV alcohol use disorders and major depression: results of a national survey. Drug and Alcohol Dependence, 39(3), 197–206. https://doi.org/10.1016/0376-8716(95)01160-4
  • Gruene, T. M., Flick, K., Stefano, A., Shea, S. D., & Shansky, R. M. (2015). Sexually divergent expression of active and passive conditioned fear responses in rats. eLife, 4, e11352. https://doi.org/10.7554/eLife.11352
  • Hamilton, G. F., Hernandez, I. J., Krebs, C. P., Bucko, P. J., & Rhodes, J. S. (2017). Neonatal alcohol exposure reduces number of parvalbumin-positive interneurons in the medial prefrontal cortex and impairs passive avoidance acquisition in mice deficits not rescued from exercise. Neuroscience, 352, 52–63. https://doi.org/10.1016/j.neuroscience.2017.03.058
  • Hermann, A., Stark, R., Milad, M. R., & Merz, C. J. (2016). Renewal of conditioned fear in a novel context is associated with hippocampal activation and connectivity. Social Cognitive and Affective Neuroscience, 11(9), 1411–1421. https://doi.org/10.1093/scan/nsw047
  • Jin, J., & Maren, S. (2015). Prefrontal-Hippocampal Interactions in Memory and Emotion. Frontiers in Systems Neuroscience, 9, 170. https://doi.org/10.3389/fnsys.2015.00170
  • Jo, Y. S., Heymann, G., & Zweifel, L. S. (2018). Dopamine Neurons Reflect the Uncertainty in Fear Generalization. Neuron, 100(4), 916–925.e3. https://doi.org/10.1016/j.neuron.2018.09.028
  • Johansen, J. P., Cain, C. K., Ostroff, L. E., & LeDoux, J. E. (2011). Molecular mechanisms of fear learning and memory. Cell, 147(3), 509–524. https://doi.org/10.1016/j.cell.2011.10.009
  • Kim, E. U., Varlinskaya, E. I., Dannenhoffer, C. A., & Spear, L. P. (2019). Adolescent intermittent ethanol exposure: Effects on pubertal development, novelty seeking, and social interaction in adulthood. Alcohol, 75, 19–29. https://doi.org/10.1016/j.alcohol.2018.05.002
  • Koss, W. A., Belden, C. E., Hristov, A. D., & Juraska, J. M. (2014). Dendritic remodeling in the adolescent medial prefrontal cortex and the basolateral amygdala of male and female rats. Synapse, 68(2), 61–72. https://doi.org/10.1002/syn.21716
  • Kyzar, E. J., Floreani, C., Teppen, T. L., & Pandey, S. C. (2016). Adolescent alcohol exposure: Burden of epigenetic reprogramming, synaptic remodeling, and adult psychopathology. Frontiers in Neuroscience, 10, 222. https://doi.org/10.3389/fnins.2016.00222
  • Marek, R., Jin, J., Goode, T. D., Giustino, T. F., Wang, Q., Acca, G. M., Holehonnur, R., Ploski, J. E., Fitzgerald, P. J., Lynagh, T., Lynch, J. W., Maren, S., & Sah, P. (2018). Hippocampus-driven feed-forward inhibition of the prefrontal cortex mediates relapse of extinguished fear. Nature Neuroscience, 21(3), 384–392. https://doi.org/10.1038/s41593-018-0073-9
  • Maren, S., & Holmes, A. (2016). Stress and Fear Extinction. Neuropsychopharmacology, 41(1), 58–79. https://doi.org/10.1038/npp.2015.180
  • Maren, S., Phan, K. L., & Liberzon, I. (2013). The contextual brain: implications for fear conditioning, extinction and psychopathology. Nature Reviews, 14(6), 417–428. https://doi.org/10.1038/nrn3492
  • McCormick, C. M. (2022). Methods and challenges in investigating sex-specific consequences of social stressors in adolescence in rats: Is it the stress or the social or the stage of development? Curr Top Behav Neurosci, 54, 23–58. https://doi.org/10.1007/7854_2021_245
  • Molas, S., Zhao-Shea, R., Liu, L., DeGroot, S. R., Gardner, P. D., & Tapper, A. R. (2017). A circuit-based mechanism underlying familiarity signaling and the preference for novelty. Nature Neuroscience, 20(9), 1260–1268. https://doi.org/10.1038/nn.4607
  • Naneix, F., Marchand, A. R., Di Scala, G., Pape, J.-R., & Coutureau, E. (2012). Parallel maturation of goal-directed behavior and dopaminergic systems during adolescence. The Journal of Neuroscience, 32(46), 16223–16232. https://doi.org/10.1523/JNEUROSCI.3080-12.2012
  • Obray, J. D., Landin, J. D., Vaughan, D. T., Scofield, M. D., & Chandler, L. J. (2022). Adolescent alcohol exposure reduces dopamine 1 receptor modulation of prelimbic neurons projecting to the nucleus accumbens and basolateral amygdala. Addiction Neuroscience, 4, 100044. https://doi.org/10.1016/j.addicn.2022.100044
  • Orsini, C. A., Kim, J. H., Knapska, E., & Maren, S. (2011). Hippocampal and prefrontal projections to the basal amygdala mediate contextual regulation of fear after extinction. The Journal of Neuroscience, 31(47), 17269–17277. https://doi.org/10.1523/JNEUROSCI.4095-11.2011
  • Pajser, A., Breen, M., Fisher, H., & Pickens, C. L. (2018). Individual differences in conditioned fear are associated with levels of adolescent/early adult alcohol consumption and instrumental extinction. Behavioural Brain Research, 349, 145–157. https://doi.org/10.1016/j.bbr.2018.04.020
  • Pajser, A., Limoges, A., Long, C., & Pickens, C. L. (2019). Individual differences in voluntary alcohol consumption are associated with conditioned fear in the fear incubation model. Behavioural Brain Research, 362, 299–310. https://doi.org/10.1016/j.bbr.2019.01.027
  • Pawlak, C. R., Ho, Y. -J., & Schwarting, R. K. W. (2008). Animal models of human psychopathology based on individual differences in novelty-seeking and anxiety. Neuroscience and Biobehavioral Reviews, 32(8), 1544–68. https://doi.org/10.1016/j.neubiorev.2008.06.007
  • Phillips, R. G., & LeDoux, J. E. (1994). Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. Learning & Memory, 1(1), 34–44. https://doi.org/10.1101/lm.1.1.34
  • Philpot, R. M., Wecker, L., & Kirstein, C. L. (2009). Repeated ethanol exposure during adolescence alters the developmental trajectory of dopaminergic output from the nucleus accumbens septi. International Journal of Developmental Neuroscience, 27(8), 805–815. https://doi.org/10.1016/j.ijdevneu.2009.08.009
  • Rohde, P., Lewinsohn, P. M., Kahler, C. W., Seeley, J. R., & Brown, R. A. (2001). Natural course of alcohol use disorders from adolescence to young adulthood. Journal of the American Academy of Child and Adolescent Psychiatry, 40(1), 83–90. https://doi.org/10.1097/00004583-200101000-00020
  • Rohde, P., Lewinsohn, P. M., & Seeley, J. R. (1996). Psychiatric comorbidity with problematic alcohol use in high school students. Journal of the American Academy of Child and Adolescent Psychiatry, 35(1), 101–109. https://doi.org/10.1097/00004583-199601000-00018
  • Rubinow, M. J., & Juraska, J. M. (2009). Neuron and glia numbers in the basolateral nucleus of the amygdala from preweaning through old age in male and female rats: A stereological study. The Journal of Comparative Neurology, 512(6), 717–725. https://doi.org/10.1002/cne.21924
  • Saddoris, M. P., Cacciapaglia, F., Wightman, R. M., & Carelli, R. M. (2015). Differential dopamine release dynamics in the nucleus accumbens core and shell reveal complementary signals for error prediction and incentive motivation. The Journal of Neuroscience, 35(33), 11572–11582. https://doi.org/10.1523/JNEUROSCI.2344-15.2015
  • Saddoris, M. P., Siletti, K. A., Stansfield, K. J., & Bercum, M. F. (2018). Heterogeneous dopamine signals support distinct features of motivated actions: Implications for learning and addiction. Learning & Memory, 25(9), 416–424. https://doi.org/10.1101/lm.047019.117
  • Sicher, A. R., Duerr, A., Starnes, W. D., & Crowley, N. A. (2022). Adolescent alcohol and stress exposure rewires key cortical neurocircuitry. Frontiers in Neuroscience, 16, 896880. https://doi.org/10.3389/fnins.2022.896880
  • Silbereis, J. C., Pochareddy, S., Zhu, Y., Li, M., & Sestan, N. (2016). The cellular and molecular landscapes of the developing human central nervous system. Neuron, 89(2), 248–268. https://doi.org/10.1016/j.neuron.2015.12.008
  • Slawecki, C. J., Betancourt, M., Cole, M., & Ehlers, C. L. (2001). Periadolescent alcohol exposure has lasting effects on adult neurophysiological function in rats. Brain Research, 128(1), 63–72. https://doi.org/10.1016/s0165-3806(01)00150-x
  • Spear, L. P. (2018). Effects of adolescent alcohol consumption on the brain and behaviour. Nature Reviews. Neuroscience, 19(4), 197–214. https://doi.org/10.1038/nrn.2018.10
  • Spear, L. P. (2015). Adolescent alcohol exposure: Are there separable vulnerable periods within adolescence? Physiology & Behavior, 148, 122–130. https://doi.org/10.1016/j.physbeh.2015.01.027
  • Spear, L. P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews, 24(4), 417–463. https://doi.org/10.1016/s0149-7634(00)00014-2
  • Spoelder, M., Tsutsui, K. T., Lesscher, H. M. B., Vanderschuren, L. J. M. J., & Clark, J. J. (2015). Adolescent alcohol exposure amplifies the incentive value of reward-predictive cues through potentiation of phasic dopamine signaling. Neuropsychopharmacology, 40(13), 2873–2885. https://doi.org/10.1038/npp.2015.139
  • Stead, J. D. H., Clinton, S., Neal, C., Schneider, J., Jama, A., Miller, S., Vazquez, D. M., Watson, S. J., & Akil, H. (2006). Selective breeding for divergence in novelty-seeking traits: heritability and enrichment in spontaneous anxiety-related behaviors. Behavior Genetics, 36(5), 697–712. https://doi.org/10.1007/s10519-006-9058-7
  • Steinberg, L., Albert, D., Cauffman, E., Banich, M., Graham, S., & Woolard, J. (2008). Age differences in sensation seeking and impulsivity as indexed by behavior and self-report: Evidence for a dual systems model. Developmental Psychology, 44(6), 1764–1778. https://doi.org/10.1037/a0012955
  • Susskind, J. M., Lee, D. H., Cusi, A., Feiman, R., Grabski, W., & Anderson, A. K. (2008). Expressing fear enhances sensory acquisition. Nature Neuroscience, 11(7), 843–850. https://doi.org/10.1038/nn.2138
  • Szumlinski, K. K., Coelho, M. A., Lee, K. M., Tran, T., Sern, K. R., Bernal, A., & Kippin, T. E. (2019). DID it or DIDn’t it? Exploration of a failure to replicate binge-like alcohol-drinking in C57BL/6J mice. Pharmacology, Biochemistry, and Behavior, 178, 3–18. https://doi.org/10.1016/j.pbb.2018.12.002
  • Tang, W., Kochubey, O., Kintscher, M., & Schneggenburger, R. (2020). A VTA to basal amygdala dopamine projection contributes to signal salient somatosensory events during fear learning. The Journal of Neuroscience, 40(20), 3969–3980. https://doi.org/10.1523/JNEUROSCI.1796-19.2020
  • Tarazi, F. I., & Baldessarini, R. J. (2000). Comparative postnatal development of dopamine D(1), D(2) and D(4) receptors in rat forebrain. International Journal of Developmental Neuroscience, 18(1), 29–37. https://doi.org/10.1016/s0736-5748(99)00108-2
  • Thiele, T. E., & Navarro, M. (2014). “Drinking in the dark” (DID) procedures: A model of binge-like ethanol drinking in non-dependent mice. Alcohol, 48(3), 235–241. https://doi.org/10.1016/j.alcohol.2013.08.005
  • Towner, T. T., & Spear, L. P. (2021). Rats exposed to intermittent ethanol during late adolescence exhibit enhanced habitual behavior following reward devaluation. Alcohol, 91, 11–20. https://doi.org/10.1016/j.alcohol.2020.09.004
  • Trantham-Davidson, H., Centanni, S. W., Garr, S. C., New, N. N., Mulholland, P. J., Gass, J. T., Glover, E. J., Floresco, S. B., Crews, F. T., Krishnan, H. R., Pandey, S. C., & Chandler, L. J. (2017). Binge-like alcohol exposure during adolescence disrupts dopaminergic neurotransmission in the adult prelimbic cortex. Neuropsychopharmacology, 42(5), 1024–1036. https://doi.org/10.1038/npp.2016.190
  • Tseng, K.-Y., & O’Donnell, P. (2007). Dopamine modulation of prefrontal cortical interneurons changes during adolescence. Cerebral Cortex, 17(5), 1235–1240. https://doi.org/10.1093/cercor/bhl034
  • Tsetsenis, T., Badyna, J. K., Wilson, J. A., Zhang, X., Krizman, E. N., Subramaniyan, M., Yang, K., Thomas, S. A., & Dani, J. A. (2021). Midbrain dopaminergic innervation of the hippocampus is sufficient to modulate formation of aversive memories. Proceedings of the National Academy of Sciences of the United States of America, 118(40), e2111069118. https://doi.org/10.1073/pnas.2111069118
  • Varlinskaya, E. I., Hosová, D., Towner, T., Werner, D. F., & Spear, L. P. (2020). Effects of chronic intermittent ethanol exposure during early and late adolescence on anxiety-like behaviors and behavioral flexibility in adulthood. Behavioural Brain Research, 378, 112292. https://doi.org/10.1016/j.bbr.2019.112292
  • Wang, Q., Jin, J., & Maren, S. (2016). Renewal of extinguished fear activates ventral hippocampal neurons projecting to the prelimbic and infralimbic cortices in rats. Neurobiology of Learning and Memory, 134(Pt A), 38–43. https://doi.org/10.1016/j.nlm.2016.04.002
  • Willing, J., Cortes, L. R., Brodsky, J. M., Kim, T., & Juraska, J. M. (2017). Innervation of the medial prefrontal cortex by tyrosine hydroxylase immunoreactive fibers during adolescence in male and female rats. Developmental Psychobiology, 59(5), 583–589. https://doi.org/10.1002/dev.21525
  • Zabik, N. L., Peters, C., Iadipaolo, A., Marusak, H. A., & Rabinak, C. A. (2023). Comparison of behavioral and brain indices of fear renewal during a standard vs. novel immersive reality Pavlovian fear extinction paradigm in healthy adults. Behavioural Brain Research, 437, 114154. https://doi.org/10.1016/j.bbr.2022.114154