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Diverse Sensitivity of RHA/Verh and RLA/Verh Rats to Emotional and Spatial Aspects of a Novel Environment as a Result of a Distinct Pattern of Neuronal Activation in the Fear/Anxiety Circuit

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Abstract

Psychogenetically selected Roman high (RHA/Verh) and Roman low (RLA/Verh) avoidance rats constitute a well-recognized model of diverse emotional reactivity. The two Swiss lines display marked behavioral and endocrine differences in reaction to a novel environment. In our study we found that these differences are accompanied by a distinct, line-specific pattern of neuronal activation within the fear/anxiety circuit. We have compared the c-Fos protein expression in the medial prefrontal cortex (mPFC), basolateral (BLA), central (CeA), medial (MeA), and cortical (CoA) nuclei of amygdala, paraventricular nucleus of the hypothalamus (PVN), and CA1, CA2, and CA3 fields of the hippocampus upon exposure to a novel situation of different stressorgeneity (open field with illuminated center, elevated plus maze, hole board test and acute restraint). Profound between-line differences in the sensitivity to emotional and spatial aspects of the behavioral challenge were observed for tests measuring spontaneous behavior. This effect seems to reflect different motivational factors driving the rat behavior, which clearly suggests that the diverse emotional reactivity of RHA/Verh and RLA/Verh rats is a result of different activation of the fear/anxiety circuit.

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References

  • Aguilar R, Gil L, Flint J, Gray JA, Dawson GR, Driscoll P, Giménez-Llort L, Escorihuela RM, Fernández-Teruel A, Tobeña A (2002) Learned fear, emotional reactivity and fear of heights: a factor analytic map from a large F(2) intercross of Roman rat strains. Brain Res Bull 57(1):17–26. doi:10.1016/S0361-9230(01)00632-3

    Article  PubMed  Google Scholar 

  • Babai P, Anokhin KV, Dolgov N, Sudakov KV (2001) Characteristics of c-fos gene expression in the brains of rats with different investigative and defensive behaviors. Neurosci Behav Physiol 31(6):583–588. doi:10.1023/A:1012360809183

    Article  PubMed  CAS  Google Scholar 

  • Bignami G (1965) Selection for high rates and low rates of avoidance conditioning in the rat. Anim Behav 13(2):221–227. doi:10.1016/0003-3472(65)90038-2

    Article  PubMed  CAS  Google Scholar 

  • Boguszewski P, Zagrodzka J (2002) Emotional changes related to age in rats: a behavioral analysis. Behav Brain Res 133(2):323–332. doi:10.1016/S0166-4328(02)00018-9

    Article  PubMed  Google Scholar 

  • Boguszewski P, Zagrodzka J (2005) Expression of c-Fos in response to stressogenic stimuli in the amygdala of old vs. young rats: a preliminary study. Acta Neurobiol Exp 65(2):191–194

    Google Scholar 

  • Boguszewski P, Meyza K, Zagrodzka J (2005) The effect of socialization on intermale behavior in old rats. In: Polish Neuroscience Society Meeting, Cracow 2005. Abstract published in Acta Neurobiologae Experimentalis, vol 65(3), p 358

  • Broadhurst PL (1975) The Maudsley reactive and nonreactive strains of rats: a survey. Behav Genet 5(4):299–319. doi:10.1007/BF01073201

    Article  PubMed  CAS  Google Scholar 

  • Campeau S, Falls WA, Cullinan WE, Helmreich DL, Davis M, Watson SJ (1997) Elicitation and reduction of fear: behavioral and neuroendocrine indices and brain induction of the immediate-early gene c-fos. Neuroscience 78(4):1087–1104. doi:10.1016/S0306-4522(96)00632-X

    Article  PubMed  CAS  Google Scholar 

  • Corda MG, Lecca D, Piras G, Di Chiara G, Giorgi O (1997) Biochemical parameters of dopaminergic and GABAergic neurotransmission in the CNS of Roman high-avoidance and Roman low-avoidance rats. Behav Genet 27(6):527–536. doi:10.1023/A:1021452814574

    Article  PubMed  CAS  Google Scholar 

  • Courvoisier H, Moisan M-P, Sarrieau A, Hendley ED, Mormède P (1996) Behavioral and neuroendocrine reactivity to stress in the WKHA/WKY inbred rat strains: a multifactorial and genetic analysis. Brain Res 743:77–85. doi:10.1016/S0006-8993(96)01023-2

    Article  PubMed  CAS  Google Scholar 

  • Cullinan WE, Herman JP, Battaglia DF, Akil H, Watson SJ (1995) Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience 64(2):477–505. doi:10.1016/0306-4522(94)00355-9

    Article  PubMed  CAS  Google Scholar 

  • Dayas CV, Buller KM, Crane JW, Xu Y, Day TA (2001) Stressor categorization: acute physical and psychological stressors elicit distinctive recruitment patterns in the amygdala and in medullary noradrenergic cell groups. The Eur J of Neurosci 14(7):1143–1152. doi:10.1046/j.0953-816x.2001.01733.x

    Article  CAS  Google Scholar 

  • Driscoll P, Bätting K (1982) Behavioral, emotional and neurochemical profiles of rats selected for extreme differences in active two-way avoidance performance. In: Lieblich I (ed) Genetics of the brain. Elsevier Biomedical, Amsterdam, pp 95–123

    Google Scholar 

  • Driscoll P, Dedek J, Martin JR, Zivkovic B (1983) Two-way avoidance and acute shock stress induced alterations of regional noradrenergic, dopaminergic and serotonergic activity in Roman high- and low-avoidance rats. Life Sci 33(17):1719–1725. doi:10.1016/0024-3205(83)90729-4

    Article  PubMed  CAS  Google Scholar 

  • Driscoll P, Escorihuela RM, Fernández-Teruel A, Giorgi O, Schwegler H, Steimer T, Wiersma A, Corda MG, Flint J, Koolhaas JM, Langhans W, Schulz PE, Siegel J, Tobeña A (1998) Genetic selection and differential stress responses. The Roman lines/strains of rats. Ann NY Acad Sci 851:501–510. doi:10.1111/j.1749-6632.1998.tb09029.x

    Article  PubMed  CAS  Google Scholar 

  • Escorihuela RM, Tobeña A, Driscoll P, Fernández-Teruel A (1995) Effects of training, early handling, and perinatal flumazenil on shuttle box acquisition in Roman low-avoidance rats: toward overcoming a genetic deficit. Neurosci Biobehav Rev 19(3):353–367. doi:10.1016/0149-7634(94)00051-2

    Article  PubMed  CAS  Google Scholar 

  • Escorihuela RM, Fernández-Teruel A, Gil L, Aguilar R, Tobeña A, Driscoll P (1999) Inbred Roman high- and low-avoidance rats: differences in anxiety, novelty-seeking, and shuttlebox behaviors. Physiol Behav 67(1):19–26. doi:10.1016/S0031-9384(99)00064-5

    Article  PubMed  CAS  Google Scholar 

  • Fernandes C, González MI, Wilson CA, File SE (1999) Factor analysis shows that female rat behavior is characterized primarily by activity, male rats are driven by sex and anxiety. Pharmacol Biochem Behav 64(4):731–738. doi:10.1016/S0091-3057(99)00139-2

    Article  PubMed  CAS  Google Scholar 

  • Fernández-Teruel A, Escorihuela RM, Núñez JF, Gomà M, Driscoll P, Tobeña A (1992) Early stimulation effects on novelty-induced behavior in two psychogenetically-selected rat lines with divergent emotionality profiles. Neurosci Lett 137(2):185–188. doi:10.1016/0304-3940(92)90400-2

    Article  PubMed  Google Scholar 

  • Ferré P, Fernández-Teruel A, Escorihuela RM, Driscoll P, Corda MG, Giorgi O, Tobeña A (1995) Behavior of the Roman/Verh high- and low-avoidance rat lines in anxiety tests: relationship with defecation and self-grooming. Physiol Behav 58(6):1209–1213. doi:10.1016/0031-9384(95)02068-3

    Article  PubMed  Google Scholar 

  • Fleming AS, Walsh C (1994) Neuropsychology of maternal behavior in the rat: c-fos expression during mother-litter interactions. Psychoneuroendocrinology 19(5–7):429–443. doi:10.1016/0306-4530(94)90030-2

    Article  PubMed  CAS  Google Scholar 

  • Fujita O, Annen Y, Kitaoka A (1994) Tsukuba high- and low-emotional strains of rats (Rattus norvegicus): an overview. Behav Genet 24(4):389–415. doi:10.1007/BF01067540

    Article  PubMed  CAS  Google Scholar 

  • Gentsch C, Lichtsteiner M, Driscoll P, Feer H (1982) Differential hormonal and physiological responses to stress in Roman high- and low-avoidance rats. Physiol Behav 28(2):259–263. doi:10.1016/0031-9384(82)90072-5

    Article  PubMed  CAS  Google Scholar 

  • Giorgi O, Orlandi M, Escorihuela RM, Driscoll P, Lecca D, Corda MG (1994) GABAergic and dopaminergic transmission in the brain of Roman high-avoidance and Roman low-avoidance rats. Brain Res 638(1–2):133–138. doi:10.1016/0006-8993(94)90642-4

    Article  PubMed  CAS  Google Scholar 

  • Giorgi O, Corda MG, Carboni G, Frau V, Valentini V, Di Chiara G (1997) Effects of cocaine and morphine in rats from two psychogenetically selected lines: a behavioral and brain dialysis study. Behav Genet 27(6):537–546. doi:10.1023/A:1021405031412

    Article  PubMed  CAS  Google Scholar 

  • Giorgi O, Piras G, Lecca D, Hansson S, Driscoll P, Corda MG (2003a) Differential neurochemical properties of central serotonergic transmission in Roman high- and low-avoidance rats. J Neurochem 86(2):422–431. doi:10.1046/j.1471-4159.2003.01845.x

    Article  PubMed  CAS  Google Scholar 

  • Giorgi O, Lecca D, Piras G, Driscoll P, Corda MG (2003b) Dissociation between mesocortical dopamine release and fear-related behaviors in two psychogenetically selected lines of rats that differ in coping strategies to aversive conditions. Eur J Neurosci 17(12):2716–2726. doi:10.1046/j.1460-9568.2003.02689.x

    Article  PubMed  CAS  Google Scholar 

  • Guitart-Masip M, Johansson B, Fernández-Teruel A, Cañete T, Tobeña A, Terenius L, Giménez-Llort L (2006) Divergent anatomical pattern of D1 and D3 binding and dopamine- and cyclic AMP-regulated phosphoprotein of 32 kDa mRNA expression in Roman rat strains: implication for drug addiction. Neuroscience 142(4):1231–1243. doi:10.1016/j.neuroscience.2006.07.041

    Article  PubMed  CAS  Google Scholar 

  • Guitart-Masip M, Johansson B, Fernández-Teruel A, Tobeña A, Giménez-Llort L (2008) Divergent effect of the selective D3 receptor agonist pd-128, 907 on locomotor activity in Roman high- and low-avoidance rats: relationship to NGFI-A gene expression in the Calleja islands. Psychopharmacology 196:39–49. doi:10.1007/s00213-007-0925-6

    Article  PubMed  CAS  Google Scholar 

  • Honkaniemi J, Kainu T, Ceccatelli S, Rechardt L, Hökfelt T, Pelto-Huikko M (1992) Fos and jun in rat central amygdaloid nucleus and paraventricular nucleus after stress. Neuroreport 3(10):849–852. doi:10.1097/00001756-199210000-00007

    Article  PubMed  CAS  Google Scholar 

  • Kabbaj M, Akil H (2001) Individual differences in novelty-seeking behavior in rats: a c-fos study. Neuroscience 106(3):535–545. doi:10.1016/S0306-4522(01)00291-3

    Article  PubMed  CAS  Google Scholar 

  • Kabbaj M, Devine DP, Savage VR, Akil H (2000) Neurobiological correlates of individual differences in novelty-seeking behavior in the rat: differential expression of stress-related molecules. J Neurosci 20(18):6983–6988

    PubMed  CAS  Google Scholar 

  • Kalueff AV (2007) Neurobiology of memory and anxiety: from genes to behavior. Neural Plasticity, 2007, 78171. Epub 2007 Jan 10

  • Kendler KS, Walters EE, Truett KR, Heath AC, Neale MC, Martin NG, Eaves LJ (1994) Sources of individual differences in depressive symptoms: analysis of two samples of twins and their families. Am J Psychiatry 151(11):1605–1614

    PubMed  CAS  Google Scholar 

  • Kjelstrup KG, Tuvnes FA, Steffenach HA, Murison R, Moser EI, Moser MB (2002) Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci USA 99(16):10825–10830. doi:10.1073/pnas.152112399

    Article  PubMed  CAS  Google Scholar 

  • Knapska E, Radwanska K, Werka T, Kaczmarek L (2007) Functional internal complexity of amygdala: focus on gene activity mapping after behavioral training and drugs of abuse. Physiol Rev 87(4):1113–1173. doi:10.1152/physrev.00037.2006

    Article  PubMed  CAS  Google Scholar 

  • Kononen J, Honkaniemi J, Alho H, Koistinaho J, Iadarola M, Pelto-Huikko M (1992) Fos-like immunoreactivity in the rat hypothalamic-pituitary axis after immobilization stress. Endocrinology 130(5):3041–3047. doi:10.1210/en.130.5.3041

    Article  PubMed  CAS  Google Scholar 

  • Kovacs KJ (1998) c-Fos as a transcription factor: a stressful (re)view from a functional map. Neurochem Int 33(4):287–297. doi:10.1016/S0197-0186(98)00023-0

    Article  PubMed  CAS  Google Scholar 

  • Landgraf R, Wigger A (2002) High vs low anxiety-related behavior rats: an animal model of extremes in trait anxiety. Behav Genet 32(5):301–314. doi:10.1023/A:1020258104318

    Article  PubMed  Google Scholar 

  • LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184. doi:10.1146/annurev.neuro.23.1.155

    Article  PubMed  CAS  Google Scholar 

  • Martin JR, Oettinger R, Driscoll P, Buzzi R, Bättig K (1982) Effects of chlordiazepoxide and imipramine on maze patrolling within two different maze configurations by psychogenetically selected lines of rats. Psychopharmacology 78(1):58–62. doi:10.1007/BF00470589

    Article  PubMed  CAS  Google Scholar 

  • Meyza KZ, Boguszewski PM, Nikolaev E, Zagrodzka J (2007) The effect of age on the dynamics and the level of c-Fos activation in response to acute restraint in Lewis rats. Behav Brain Res 180(2):183–189. doi:10.1016/j.bbr.2007.03.007

    Article  PubMed  CAS  Google Scholar 

  • Moser EI, Kropff E, Moser MB (2008) Place cells, grid cells, and the brain’s spatial representation system. Annu Rev Neurosci 31 (Epub ahead of print)

  • Mulders WH, Meek J, Schmidt ED, Hafmans TG, Cools AR (1995) The hypothalamic paraventricular nucleus in two types of Wistar rats with different stress responses. II. Differential Fos-expression. Brain Res 689(1):61–70. doi:10.1016/0006-8993(95)00546-3

    Article  PubMed  CAS  Google Scholar 

  • Ohl F, Holsboer F, Landgraf R (2001) The modified hole board as a differential screen for behavior in rodents. Behav Res Methods Instrum Comput 33(3):392–397

    PubMed  CAS  Google Scholar 

  • Pace TW, Gaylord R, Topczewski F, Girotti M, Rubin B, Spencer RL (2005) Immediate-early gene induction in hippocampus and cortex as a result of novel experience is not directly related to the stressfulness of that experience. Eur J Neurosci 22(7):1679–1690. doi:10.1111/j.1460-9568.2005.04354.x

    Article  PubMed  Google Scholar 

  • Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates, 3rd edn. Academic Press, New York

    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(3):149–167. doi:10.1016/0165-0270(85)90031-7

    Article  PubMed  CAS  Google Scholar 

  • Pezzone MA, Lee WS, Hoffman GE, Rabin BS (1992) Induction of c-Fos immunoreactivity in the rat forebrain by conditioned and unconditioned aversive stimuli. Brain Res 597(1):41–50. doi:10.1016/0006-8993(92)91503-7

    Article  PubMed  CAS  Google Scholar 

  • Pfaus JG, Heeb MM (1997) Implications of immediate-early gene induction in the brain following sexual stimulation of female and male rodents. Brain Res Bull 44(4):397–407. doi:10.1016/S0361-9230(97)00219-0

    Article  PubMed  CAS  Google Scholar 

  • Pisula W (2003) The Roman high- and low-avoidance rats respond differently to novelty in a familiarized environment. Behav Process 63(2):63–72. doi:10.1016/S0376-6357(03)00032-9

    Article  Google Scholar 

  • Pisula W, Osiński JT (2000) A comparative study of the behavioral patterns of RLA/Verh and RHA/Verh rats in the exploration box. Behav Genet 30(5):375–384. doi:10.1023/A:1002748521117

    Article  PubMed  CAS  Google Scholar 

  • Ramos A, Berton O, Mormède P, Chaouloff F (1997) A multiple-test study of anxiety-related behaviors in six inbred rat strains. Behav Brain Res 85(1):57–69. doi:10.1016/S0166-4328(96)00164-7

    Article  PubMed  CAS  Google Scholar 

  • Rodgers RJ, Johnson NJ (1995) Factor analysis of spatiotemporal and ethological measures in the murine elevated plus-maze test of anxiety. Pharmacol Biochem Behav 52(2):297–303. doi:10.1016/0091-3057(95)00138-M

    Article  PubMed  CAS  Google Scholar 

  • Roozendaal B, Wiersma A, Driscoll P, Koolhaas JM, Bohus B (1992) Vasopressinergic modulation of stress responses in the central amygdala of the Roman high-avoidance and low-avoidance rat. Brain Res 596(1–2):35–40. doi:10.1016/0006-8993(92)91529-N

    Article  PubMed  CAS  Google Scholar 

  • Ryabinin AE, Wang YM, Bachtell RK, Kinney AE, Grubb MC, Mark GP (2000) Cocaine- and alcohol-mediated expression of inducible transcription factors is blocked by pentobarbital anesthesia. Brain Res 877(2):251–261. doi:10.1016/S0006-8993(00)02681-0

    Article  PubMed  CAS  Google Scholar 

  • Salomé N, Salchner P, Viltart O, Sequeira H, Wigger A, Landgraf R, Singewald N (2004) Neurobiological correlates of high (HAB) versus low anxiety-related behavior (LAB): differential Fos expression in HAB and LAB rats. Biol Psychiatry 55(7):715–723. doi:10.1016/j.biopsych.2003.10.021

    Article  PubMed  Google Scholar 

  • Savonenko A, Filipkowski RK, Werka T, Zielinski K, Kaczmarek L (1999) Defensive conditioning-related functional heterogeneity among nuclei of the rat amygdala revealed by c-Fos mapping. Neuroscience 94(3):723–733. doi:10.1016/S0306-4522(99)00331-0

    Article  PubMed  CAS  Google Scholar 

  • Schwegler H, Pilz PK, Koch M, Fendt M, Linke R, Driscoll P (1997) The acoustic startle response in inbred Roman high- and low-avoidance rats. Behav Genet 27(6):579–582. doi:10.1023/A:1021465217299

    Article  PubMed  CAS  Google Scholar 

  • Siegel J, Sisson DF, Driscoll P (1993) Augmenting and reducing of visual evoked potentials in Roman high- and low-avoidance rats. Physiol Behav 54(4):707–711. doi:10.1016/0031-9384(93)90080-Y

    Article  PubMed  CAS  Google Scholar 

  • Silveira MC, Sandner G, Graeff FG (1993) Induction of Fos immunoreactivity in the brain by exposure to the elevated plus-maze. Behav Brain Res 56(1):115–118. doi:10.1016/0166-4328(93)90028-O

    Article  PubMed  CAS  Google Scholar 

  • Singewald N, Salchner P, Sharp T (2003) Induction of c-Fos expression in specific areas of the fear circuitry in rat forebrain by anxiogenic drugs. Biol Psychiatry 53(4):275–283. doi:10.1016/S0006-3223(02)01574-3

    Article  PubMed  CAS  Google Scholar 

  • Steimer T, Driscoll P (2003) Divergent stress responses and coping styles in psychogenetically selected Roman high-(RHA) and low-(RLA) avoidance rats: behavioral, neuroendocrine and developmental aspects. Stress (Amsterdam, Netherlands) 6(2):87–100. doi:10.1080/1025389031000111320

    CAS  Google Scholar 

  • Steimer T, Driscoll P (2005) Inter-individual vs line/strain differences in psychogenetically selected Roman High-(RHA) and Low-(RLA) Avoidance rats: neuroendocrine and behavioral aspects. Neurosci Biobehav Rev 29(1):99–112. doi:10.1016/j.neubiorev.2004.07.002

    Article  PubMed  Google Scholar 

  • Steimer T, la Fleur S, Schulz PE (1997) Neuroendocrine correlates of emotional reactivity and coping in male rats from the Roman high (RHA/Verh)- and low (RLA/Verh)-avoidance lines. Behav Genet 27(6):503–512. doi:10.1023/A:1021448713665

    Article  PubMed  CAS  Google Scholar 

  • Walker CD, Rivest RW, Meaney MJ, Aubert ML (1989) Differential activation of the pituitary-adrenocortical axis after stress in the rat: use of two genetically selected lines (Roman low- and high-avoidance rats) as a model. J Endocrinol 123(3):477–485

    Article  PubMed  CAS  Google Scholar 

  • Whimbey AE, Denenberg VH (1967) Two independent behavioral dimensions in open-field performance. J Comp Physiol Psychol 63(3):500–504. doi:10.1037/h0024620

    Article  PubMed  CAS  Google Scholar 

  • Wichers M, Myin-Germeys I, Jacobs N, Peeters F, Kenis G, Derom C, Vlietinck R, Delespaul P, Van Os J (2007) Genetic risk of depression and stress-induced negative affect in daily life. Br J Psychiatry 191:218–223. doi:10.1192/bjp.bp.106.032201

    Article  PubMed  Google Scholar 

  • Wiersma A, Knollema S, Konsman JP, Bohus B, Koolhaas JM (1997) Corticotropin-releasing hormone modulation of a conditioned stress response in the central amygdala of Roman high (RHA/Verh)-avoidance and low (RLA/Verh)-avoidance rats. Behav Genet 27(6):547–555. doi:10.1023/A:1021457015482

    Article  PubMed  CAS  Google Scholar 

  • Wigger A, Loerscher P, Weissenbacher P, Holsboer F, Landgraf R (2001) Cross-fostering and cross-breeding of HAB and LAB rats: a genetic rat model of anxiety. Behav Genet 31(4):371–382. doi:10.1023/A:1012222402346

    Article  PubMed  CAS  Google Scholar 

  • Yilmazer-Hanke DM, Faber-Zuschratter H, Linke R, Schwegler H (2002) Contribution of amygdala neurons containing peptides and calcium-binding proteins to fear-potentiated startle and exploration-related anxiety in inbred Roman high- and low-avoidance rats. Eur J Neurosci 15(7):1206–1218. doi:10.1046/j.1460-9568.2002.01945.x

    Article  PubMed  Google Scholar 

  • Zeier H, Bättig K, Driscoll P (1978) Acquisition of DRL-20 bahvior in male and female Roman high- and low-avoidance rats. Physiol Behav 20:791–793. doi:10.1016/0031-9384(78)90307-4

    Article  PubMed  CAS  Google Scholar 

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Acknowledegments

We would like to thank Dr. Thierry Steimer from the Laboratoire de Recherches Unité de Psychopharmacologie Clinique (APSIC), Hôpitaux Universitaires de Geneve for generous donation of Roman High Avoidance (RHA/Verh) and Roman Low Avoidance (RLA/Verh) for this study. We would also like to thank Dr. Ewelina Knapska and Dr. Mark Hunt for their comments on the manuscript and Maciek Olszewski for the technical assistance. This work was supported by State Committee for Scientific Research (KBN) grant no. 2PO4C03826.

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  1. Department of Neurophysiology, Nencki Institute of Experimental Biology, Polish Academy of Sciences, 3 Pasteur Street, 02-093, Warsaw, Poland

    Ksenia Z. Meyza & Jolanta Zagrodzka

  2. Department of Psychology, Yale University, 2 Hillhouse Ave., New Haven, CT, 06520-8205, USA

    Pawel M. Boguszewski

  3. Department of Molecular and Cellular Neurobiology, Nencki Institute of Experimental Biology, Polish Academy of Sciences, 3 Pasteur Street, 02-093, Warsaw, Poland

    Evgeni Nikolaev

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  1. Ksenia Z. Meyza
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Correspondence to Jolanta Zagrodzka.

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Meyza, K.Z., Boguszewski, P.M., Nikolaev, E. et al. Diverse Sensitivity of RHA/Verh and RLA/Verh Rats to Emotional and Spatial Aspects of a Novel Environment as a Result of a Distinct Pattern of Neuronal Activation in the Fear/Anxiety Circuit. Behav Genet 39, 48–61 (2009). https://doi.org/10.1007/s10519-008-9234-z

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