Juvenile stress potentiates aversive 22-kHz ultrasonic vocalizations and freezing during auditory fear conditioning in adult male rats

References

• Andersen SL. 2003. Trajectories of brain development: Point of vulnerability or window of opportunity?. Neurosci Biobehav Rev. 27:3–18.
   PubMed Web of Science ®Google Scholar
• Antoniadis EA, McDonald RJ. 1999. Discriminative fear conditioning to context expressed by multiple measures of fear in the rat. Behav Brain Res. 101:1–13.
   PubMed Web of Science ®Google Scholar
• Avital A, Richter-Levin G. 2005. Exposure to juvenile stress exacerbates the behavioural consequences of exposure to stress in the adult rat. Int J Neuropsychopharmacol. 8:163–173.
   PubMed Web of Science ®Google Scholar
• Bazak N, Kozlovsky N, Kaplan Z, Matar M, Golan H, Zohar J, Richter-Levin G., Cohen H.. 2009. Pre-pubertal stress exposure affects adult behavioral response in association with changes in circulating corticosterone and brain-derived neurotrophic factor. Psychoneuroendocrinology. 34:844–858.
   PubMed Web of Science ®Google Scholar
• Bingham B, McFadden K, Zhang X, Bhatnagar S, Beck S, Valentino R. 2010. Early adolescence as a critical window during which social stress distinctly alters behavior and brain norepinephrine activity. Neuropsychopharmacology. 36:896–909.
   PubMed Web of Science ®Google Scholar
• Blanchard RJ, Blanchard DC. 1969. Crouching as an index of fear. J Comp Physiol Psychol. 67:370–375.
   PubMed Web of Science ®Google Scholar
• Blanchard RJ, Blanchard DC. 1971. Defensive reactions in the Albino rat. Learn Motiv. 2:351–362.
   Google Scholar
• Blanchard RJ, Blanchard DC, Agullana R, Weiss SM. 1991. Twenty-two kHz alarm cries to presentation of a predator, by laboratory rats living in visible burrow systems. Physiol Behav. 50:967–972.
   PubMed Web of Science ®Google Scholar
• Borta A, Wöhr M, Schwarting RKW. 2006. Rat ultrasonic vocalization in aversively motivated situations and the role of individual differences in anxiety-related behavior. Behav Brain Res. 166:271–280.
   PubMed Web of Science ®Google Scholar
• Bourke CH, Neigh GN. 2011. Behavioral effects of chronic adolescent stress are sustained and sexually dimorphic. Horm Behav. 60:112–120.
   PubMed Web of Science ®Google Scholar
• Brudzynski SM. 2001. Pharmacological and behavioral characteristics of 22 kHz alarm calls in rats. Neurosci Biobehav Rev. 25:611–617.
   Google Scholar
• Choi JS, Brown TH. 2003. Central amygdala lesions block ultrasonic vocalization and freezing as conditional but not unconditional responses. J Neurosci. 23:8713–8721.
   PubMed Web of Science ®Google Scholar
• Conrad CD, LeDoux JE, Magarinos AM, McEwen BS. 1999. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav Neurosci. 113:902–913.
   PubMed Web of Science ®Google Scholar
• Cordero MI, Kruyt ND, Sandi C. Modulation of contextual fear conditioning by chronic stress in rats is related to individual differences in behavioral reactivity to novelty. Brain Res. 2003a; 970:242–245.
   PubMed Web of Science ®Google Scholar
• Cordero MI, Venero C, Kruyt ND, Sandi C. Prior exposure to a single stress session facilitates subsequent contextual fear conditioning in rats. Evidence for a role of corticosterone. Horm Behav. 2003b; 44:338–345.
   PubMed Web of Science ®Google Scholar
• De Vry J, Benz U, Schreiber R, Traber J. 1993. Shock-induced ultrasonic vocalization in young adult rats: A model for testing putative anti-anxiety drugs. Eur J Pharmacol. 249:331–339.
   PubMed Web of Science ®Google Scholar
• Endres T, Widmann K, Fendt M. 2007. Are rats predisposed to learn 22 kHz calls as danger-predicting signals?. Behav Brain Res. 185:69–75.
   PubMed Web of Science ®Google Scholar
• Fendt M, Fanselow MS. 1999. The neuroanatomical and neurochemical basis of conditioned fear. Neurosci Biobehav Rev. 23:743–760.
   PubMed Web of Science ®Google Scholar
• Foilb A, Lui P, Romeo R. 2011. The transformation of hormonal stress responses throughout puberty and adolescence. J Endocrinol. 210:391–398.
   PubMed Web of Science ®Google Scholar
• Hamed A, Jaroszewski T, Maciejak P, Szyndler J, Lehner M, Kamecka I, . 2009. The effects of buspirone and diazepam on aversive context- and social isolation-induced ultrasonic vocalisation. Physiol Behav. 98:474–480.
   PubMed Web of Science ®Google Scholar
• Harmon KM, Greenwald ML, McFarland A, Beckwith T, Cromwell HC. 2009. The effects of prenatal stress on motivation in the rat pup. Stress. 12:250–258.
   PubMed Web of Science ®Google Scholar
• Heim C, Nemeroff CB. 2001. The role of childhood trauma in the neurobiology of mood and anxiety disorders: Preclinical and clinical studies. Biol Psychiatry. 49:1023–1039.
   PubMed Web of Science ®Google Scholar
• Ilin Y, Richter-Levin G. 2009. Enriched environment experience overcomes learning deficits and depressive-like behavior induced by juvenile stress. PLoS ONE. 4:e4329.
   PubMed Web of Science ®Google Scholar
• Jacobson-Pick S, Richter-Levin G. 2010. Differential impact of juvenile stress and corticosterone in juvenility and in adulthood, in male and female rats. Behav Brain Res. 214:268–276.
   PubMed Web of Science ®Google Scholar
• Jankord R, Solomon MB, Albertz J, Flak JN, Zhang R, Herman JP. 2011. Stress vulnerability during adolescent development in rats. Endocrinology. 152:629–638.
   PubMed Web of Science ®Google Scholar
• Jelen P, Soltysik S, Zagrodzka J. 2003. 22-kHz ultrasonic vocalization in rats as an index of anxiety but not fear: Behavioral and pharmacological modulation of affective state. Behav Brain Res. 141:63–72.
   PubMed Web of Science ®Google Scholar
• Kendler KS, Karkowski LM, Prescott CA. 1999. Causal relationship between stressful life events and the onset of major depression. Am J Psychiatry. 156:837–841.
   PubMed Web of Science ®Google Scholar
• Kikusui T, Nishizawa D, Takeuchi Y, Mori Y. 2003. Conditioned fear-related ultrasonic vocalizations are emitted as an emotional response. J Vet Med Sci. 65:1299–1305.
   PubMed Web of Science ®Google Scholar
• Knutson B, Burgdorf J, Panksepp J. 1998. Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats. J Comp Psychol. 112:65–73.
   PubMed Web of Science ®Google Scholar
• Knutson B, Burgdorf J, Panksepp J. 1999. High-frequency ultrasonic vocalizations index conditioned pharmacological reward in rats. Physiol Behav. 66:639–643.
   PubMed Web of Science ®Google Scholar
• Knutson B, Burgdorf J, Panksepp J. 2002. Ultrasonic vocalizations as indices of affective states in rats. Psychol Bull. 128:961–977.
   PubMed Web of Science ®Google Scholar
• Kosten TA, Lee HJ, Kim JJ. 2006. Early life stress impairs fear conditioning in adult male and female rats. Brain Res. 1087:142–150.
   PubMed Web of Science ®Google Scholar
• Kosten TA, Miserendino MJ, Bombace JC, Lee HJ, Kim JJ. 2005. Sex-selective effects of neonatal isolation on fear conditioning and foot shock sensitivity. Behav Brain Res. 157:235–244.
   PubMed Web of Science ®Google Scholar
• Lehmann J, Pryce CR, Bettschen D, Feldon J. 1999. The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol Biochem Behav. 64:705–715.
   PubMed Web of Science ®Google Scholar
• Litvin Y, Blanchard DC, Blanchard RJ. 2007. Rat 22 kHz ultrasonic vocalizations as alarm cries. Behav Brain Res. 182:166–172.
   PubMed Web of Science ®Google Scholar
• Maggio N, Segal M. 2011. Persistent changes in ability to express long-term potentiation/depression in the rat hippocampus after juvenile/adult stress. Biol Psychiatry. 69:748–753.
   PubMed Web of Science ®Google Scholar
• Mällo T, Matrov D, Koiv K, Harro J. 2009. Effect of chronic stress on behavior and cerebral oxidative metabolism in rats with high or low positive affect. Neuroscience. 164:963–974.
   PubMed Web of Science ®Google Scholar
• Maren S. 2001. Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci. 24:897–931.
   PubMed Web of Science ®Google Scholar
• McCormick CM, Mathews IZ. 2007. HPA function in adolescence: Role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacol Biochem Behav. 86:220–233.
   PubMed Web of Science ®Google Scholar
• McCormick CM, Mathews IZ, Thomas C, Waters P. Investigations of HPA function and the enduring consequences of stressors in adolescence in animal models. Brain Cogn. 2010a; 72:73–85.
   PubMed Web of Science ®Google Scholar
• McCormick CM, Nixon F, Thomas C, Lowie B, Dyck J. Hippocampal cell proliferation and spatial memory performance after social instability stress in adolescence in female rats. Behav Brain Res. 2010b; 208:23–29.
   PubMed Web of Science ®Google Scholar
• McCormick CM, Smith C, Mathews IZ. 2008. Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav Brain Res. 187:228–238.
   PubMed Web of Science ®Google Scholar
• Meerlo P, Horvath KM, Nagy GM, Bohus B, Koolhaas JM. 1999. The influence of postnatal handling on adult neuroendocrine and behavioural stress reactivity. J Neuroendocrinol. 11:925–933.
   PubMed Web of Science ®Google Scholar
• Molewijk HE, van der Poel AM, Mos J, van der Heyden JA, Olivier B. 1995. Conditioned ultrasonic distress vocalizations in adult male rats as a behavioural paradigm for screening anti-panic drugs. Psychopharmacology (Berl). 117:32–40.
   PubMed Web of Science ®Google Scholar
• Morgan KN, Thayer JE, Frye CA. 1999. Prenatal stress suppresses rat pup ultrasonic vocalization and myoclonic twitching in response to separation. Dev Psychobiol. 34:205–215.
   PubMed Web of Science ®Google Scholar
• Morrissey MD, Mathews IZ, McCormick CM. 2011. Enduring deficits in contextual and auditory fear conditioning after adolescent, not adult, social instability stress in male rats. Neurobiol Learn Mem. 95:46–56.
   PubMed Web of Science ®Google Scholar
• Oztan O, Aydin C, Isgor C. 2011. Stressful environmental and social stimulation in adolescence causes antidepressant-like effects associated with epigenetic induction of the hippocampal BDNF and mossy fibre sprouting in the novelty-seeking phenotype. Neurosci Lett. 501:107–111.
   PubMed Web of Science ®Google Scholar
• Pellow S, Chopin P, File SE, Briley M. 1985. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods. 14:149–167.
   PubMed Web of Science ®Google Scholar
• Pohl J, Olmstead MC, Wynne-Edwards KE, Harkness K, Menard JL. 2007. Repeated exposure to stress across the childhood-adolescent period alters rats' anxiety- and depression-like behaviors in adulthood: The importance of stressor type and gender. Behav Neurosci. 121:462–474.
   PubMed Web of Science ®Google Scholar
• Pryce CR, Bettschen D, Nanz-Bahr NI, Feldon J. 2003. Comparison of the effects of early handling and early deprivation on conditioned stimulus, context, and spatial learning and memory in adult rats. Behav Neurosci. 117:883–893.
   PubMed Web of Science ®Google Scholar
• Ricon T, Toth E, Leshem M, Braun K, Richter-Levin G. 2012. Unpredictable chronic stress in juvenile or adult rats has opposite effects, respectively, promoting and impairing resilience. Stress. 15:11–20.
   PubMed Web of Science ®Google Scholar
• Romeo RD. 2010. Adolescence: A central event in shaping stress reactivity. Dev Psychobiol. 52:244–253.
   PubMed Web of Science ®Google Scholar
• Romeo RD, Bellani R, Karatsoreos IN, Chhua N, Vernov M, Conrad CD, . 2006. Stress history and pubertal development interact to shape hypothalamic-pituitary-adrenal axis plasticity. Endocrinology. 147:1664–1674.
   PubMed Web of Science ®Google Scholar
• Romeo RD, McEwen BS. 2006. Stress and the adolescent brain. Ann NY Acad Sci. 1094:202–214.
   PubMed Web of Science ®Google Scholar
• Sales GD. 1972. Ultrasound and aggressive behaviour in rats and other small mammals. Anim Behav. 20:88–100.
   PubMed Web of Science ®Google Scholar
• Sanchez C. 2003. Stress-induced vocalisation in adult animals. A valid model of anxiety?. Eur J Pharmacol. 463:133–143.
   PubMed Web of Science ®Google Scholar
• Sandi C, Merino JJ, Cordero MI, Touyarot K, Venero C. 2001. Effects of chronic stress on contextual fear conditioning and the hippocampal expression of the neural cell adhesion molecule, its polysialylation, and L1. Neuroscience. 102:329–339.
   PubMed Web of Science ®Google Scholar
• Schwarting RKW, Jegan N, Wöhr M. 2007. Situational factors, conditions and individual variables which can determine ultrasonic vocalizations in male adult Wistar rats. Behav Brain Res. 182:208–222.
   PubMed Web of Science ®Google Scholar
• Spear L. 2000. Modeling adolescent development and alcohol use in animals. Alcohol Res Health. 24:115–123.
   PubMedGoogle Scholar
• Swiergiel AH, Zhou Y, Dunn AJ. 2007. Effects of chronic footshock, restraint and corticotropin-releasing factor on freezing, ultrasonic vocalization and forced swim behavior in rats. Behav Brain Res. 183:178–187.
   PubMed Web of Science ®Google Scholar
• Toledo-Rodriguez M, Sandi C. 2007. Stress before puberty exerts a sex- and age-related impact on auditory and contextual fear conditioning in the rat. Neural Plast. 2007:71203.
   PubMedGoogle Scholar
• Toth E, Gersner R, Wilf-Yarkoni A, Raizel H, Dar DE, Richter-Levin G, . 2008. Age-dependent effects of chronic stress on brain plasticity and depressive behavior. J Neurochem. 107:522–532.
   PubMed Web of Science ®Google Scholar
• Tsoory M, Cohen H, Richter-Levin G. 2007. Juvenile stress induces a predisposition to either anxiety or depressive-like symptoms following stress in adulthood. Eur Neuropsychopharmacol. 17:245–256.
   PubMed Web of Science ®Google Scholar
• Tsoory M, Guterman A, Richter-Levin G. 2008. Exposure to stressors during juvenility disrupts development-related alterations in the PSA-NCAM to NCAM expression ratio: Potential relevance for mood and anxiety disorders. Neuropsychopharmacology. 33:378–393.
   PubMed Web of Science ®Google Scholar
• Tsoory M, Richter-Levin G. 2006. Learning under stress in the adult rat is differentially affected by ‘juvenile’ or ‘adolescent’ stress. Int J Neuropsychopharmacol. 9:713–728.
   PubMed Web of Science ®Google Scholar
• Tsoory MM, Guterman A, Richter-Levin G. 2010. “Juvenile stress” alters maturation-related changes in expression of the neural cell adhesion molecule L1 in the limbic system: Relevance for stress-related psychopathologies. J Neurosci Res. 88:369–380.
   PubMed Web of Science ®Google Scholar
• van der Poel AM, Miczek KA. 1991. Long ultrasonic calls in male rats following mating, defeat and aversive stimulation: Frequency modulation and bout structure. Behaviour. 119:127–142.
   Web of Science ®Google Scholar
• van der Poel AM, Noach EJ, Miczek KA. 1989. Temporal patterning of ultrasonic distress calls in the adult rat: Effects of morphine and benzodiazepines. Psychopharmacology (Berl). 97:147–148.
   PubMed Web of Science ®Google Scholar
• Vidal J, Bie J, Granneman RA, Wallinga AE, Koolhaas JM, Buwalda B. 2007. Social stress during adolescence in Wistar rats induces social anxiety in adulthood without affecting brain monoaminergic content and activity. Physiol Behav. 92:824–830.
   PubMed Web of Science ®Google Scholar
• Weintraub A, Singaravelu J, Bhatnagar S. 2010. Enduring and sex-specific effects of adolescent social isolation in rats on adult stress reactivity. Brain Res. 1343:83–92.
   PubMed Web of Science ®Google Scholar
• Williams MT, Hennessy MB, Davis HN. 1998. Stress during pregnancy alters rat offspring morphology and ultrasonic vocalizations. Physiol Behav. 63:337–343.
   PubMed Web of Science ®Google Scholar
• Wöhr M, Borta A, Schwarting RKW. 2005. Overt behavior and ultrasonic vocalization in a fear conditioning paradigm: A dose-response study in the rat. Neurobiol Learn Mem. 84:228–240.
   PubMed Web of Science ®Google Scholar
• Wöhr M, Schwarting RKW. 2007. Ultrasonic communication in rats: Can playback of 50-kHz calls induce approach behavior?. PLoS ONE. 2:e1365.
   Web of Science ®Google Scholar
• Wöhr M, Schwarting RKW. Maternal care, isolation-induced infant ultrasonic calling, and their relations to adult anxiety-related behavior in the rat. Behav Neurosci. 2008a; 122:310–330.
   PubMed Web of Science ®Google Scholar
• Wöhr M, Schwarting RKW. Ultrasonic calling during fear conditioning in the rat: No evidence for an audience effect. Anim Behav. 2008b; 76:749–760.
   Web of Science ®Google Scholar
• Wöhr M, Schwarting RKW. 2009. Activation of limbic system structures by replay of ultrasonic vocalization in rats. In: Brudzynski SM. editors. Handbook of mammalian vocalization. Oxford: Academic Press113–124.
   Google Scholar
• Yee N, Plassmann K, Fuchs E. 2011. Juvenile stress impairs body temperature regulation and augments anticipatory stress-induced hyperthermia responses in rats. Physiol Behav. 104:408–416.
   PubMed Web of Science ®Google Scholar
• Young EA, Abelson JL, Curtis GC, Nesse RM. 1997. Childhood adversity and vulnerability to mood and anxiety disorders. Depress Anxiety. 5:66–72.
   PubMedGoogle Scholar