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Differential ultrasonic indices of separation distress in the presence and absence of maternal cues in infant rats bred for high and low positive social affect

Published online by Cambridge University Press:  11 March 2013

Paolo Iacobucci
Affiliation:
Department of VCAPP, College of Veterinary Medicine, Washington State University, Pullman, USA Department of Psychology, University of Rome ‘Sapienza’, Rome, Italy
Valentina Colonnello
Affiliation:
Department of VCAPP, College of Veterinary Medicine, Washington State University, Pullman, USA Department of Psychology, University of Rome ‘Sapienza’, Rome, Italy
Thomas Fuchs
Affiliation:
Department of VCAPP, College of Veterinary Medicine, Washington State University, Pullman, USA
Laura D'Antuono
Affiliation:
Department of VCAPP, College of Veterinary Medicine, Washington State University, Pullman, USA Department of Psychology, University of Rome ‘Sapienza’, Rome, Italy
Jaak Panksepp*
Affiliation:
Department of VCAPP, College of Veterinary Medicine, Washington State University, Pullman, USA
*
Jaak Panksepp, Department of VCAPP, College of Veterinary Medicine, Washington State University, Pullman, WA 99164-6520, USA. Tel: 509-335-5803; Fax: 509-335-4650; E-mail: jpanksepp@vetmed.wsu.edu

Abstract

Objective

Preclinical models of human mood disorders commonly focus on the study of negative affectivity, without comparably stressing the role of positive affects and their ability to promote resilient coping styles. We evaluated the role of background constitutional affect of rats by studying the separation and reunion responses of infants from low and high positive affect genetic lines (i.e., differentially selected for High and Low 50 kHz ultrasonic vocalisations (USVs).

Methods

Infants from Low and High 50 kHz USV breeding lines were isolated from mothers and exposed to either social (familiar or unfamiliar bedding) or neutral (clean bedding) odour cues between two short isolation periods, and tested in homeothermic and hypothermic ambient temperatures. Negative affect was estimated by monitoring separation distress calls (35–45 kHz USVs).

Results

Low Line pups called at higher rates than High Line, and their rates were stable regardless of odour cue. In contrast, High Line pups increased vocalisations during the second compared with the first isolation periods and during exposure to both familiar and unfamiliar odour cues, but not to neutral odour. Furthermore, the greatest increase in USV emission was seen in the second isolation period following exposure to the unfamiliar odour. However, both lines showed comparable elevated distress USVs to the thermal stressor.

Conclusion

High Line animals, selected for a positive affective phenotype (50 kHz USVs), exhibited reduced separation anxiety responses in infancy, making this a promising animal model for the role of constitutional affective states in emotional responsivity and potential resilience against emotional disorders.

Type
Original Articles
Copyright
Copyright © Scandinavian College of Neuropsychopharmacology 2013 

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References

1.Burgdorf, J, Panksepp, J, Brudzynski, SM, Kroes, R, Moskal, JR. Breeding for 50-kHz positive affective vocalization in rats. Behav Genet 2005;35:6772.CrossRefGoogle ScholarPubMed
2.Wöhr, M, Dahlhoff, M, Wolf, E, Holsboer, F, Schwarting, RK, Wotjak, CT. Effects of genetic background, gender, and early environmental factors on isolation-induced ultrasonic calling in mouse pups: an embryo-transfer study. Behav Genet 2008;38:579595.CrossRefGoogle ScholarPubMed
3.Moles, A, Kieffer, BL, D'amato, FR. Deficit in attachment behavior in mice lacking the mu-opioid receptor gene. Science 2004;304:19831986.CrossRefGoogle ScholarPubMed
4.Steimer, T, La Fleur, S, Schulz, PE. Neuroendocrine correlates of emotional reactivity and coping in male rats from the roman high (RHA/Verh)-and low (RLA/Verh)-avoidance lines. Behav Genet 2001;27:503512.CrossRefGoogle Scholar
5.Hofer, MA, Shair, HN, Masmela, JR, Brunelli, SA. Developmental effects of selective breeding for an infantile trait: the rat pup ultrasonic isolation call. Dev Psychobiol 2001;39:231246.CrossRefGoogle ScholarPubMed
6.Dichter, GS, Brunelli, SA, Hofer, MA. Elevated plus-maze behavior in adult-offspring of selectively bred rats. Physiol Behav 1996;60:299304.CrossRefGoogle ScholarPubMed
7.Knutson, B, Burgdorf, J, Panksepp, J. Ultrasonic vocalizations as indices of affective states in rats. Psychol Bull 2002;128:961977.CrossRefGoogle ScholarPubMed
8.Panksepp, J. Beyond a joke: from animal laughter to human joy? Science 2005;308:6263.CrossRefGoogle ScholarPubMed
9.Panksepp, J. Neuroevolutionary sources of laughter and social joy: modeling primal human laughter in laboratory rats. Behav Brain Res 2007;182:231244.CrossRefGoogle ScholarPubMed
10.Burgdorf, J, Kroes, RA, Moskal, JR, Pfaus, JG, Brudzynski, SM, Panksepp, J. Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: behavioral concomitants, relationship to reward, and self-administration of playback. J Comp Psychol 2008;122:357367.CrossRefGoogle ScholarPubMed
11.Borta, A, Wöhr, M, Schwarting, RK. Rat ultrasonic vocalization in aversively motivated situations and the role of individual differences in anxiety-related behavior. Behav Brain Res 2006;166:271280.CrossRefGoogle ScholarPubMed
12.Nitschke, W, Bell, RW, Bell, NJ, Zachman, T. The ontogeny of ultrasounds in two strains of Rattus norvegicus. Exp Aging Res 1975;1:229243.CrossRefGoogle ScholarPubMed
13.Ehret, G. Infant rodent ultrasounds-A gate to the understanding of sound communication. Behav Genet 2005;35:1929.CrossRefGoogle Scholar
14.Hofer, MA. Multiple regulators of ultrasonic vocalization in the infant rat. Psychoneuroendocr 1996;21:203217.CrossRefGoogle ScholarPubMed
15.Shair, HN. Acquisition and expression of a socially mediated separation response. Behav Brain Res 2007;182:180192.CrossRefGoogle ScholarPubMed
16.Brunelli, SA, Hofer, MA. Selective breeding for infant rat separation-induced ultrasonic vocalizations: developmental precursors of passive and active coping styles. Behav Brain Res 2007;182:193207.CrossRefGoogle ScholarPubMed
17.Panksepp, J. The riddle of laughter: Neural and psychoevolutionary underpinnings of joy. Curr Dir Psychol Sci 2000;9:183186.CrossRefGoogle Scholar
18.Panksepp, J, Burgdorf, J. The neurobiology of positive emotions. Neurosci Biobehav Rev 2006;30:173187.Google Scholar
19.Burgdorf, J, Wood, PL, Kroes, RA, Moskal, JR, Panksepp, J. Neuro-biology of 50-kHz ultrasonic vocalizations in rats: electrode mapping, lesion, and pharmacology studies. Behav Brain Res 2007;182:274283.CrossRefGoogle Scholar
20.Harmon, KM, Cromwell, HC, Burgdorf, Jet al. Rats selectively bred for low levels of 50 kHz ultrasonic vocalizations exhibit alterations in early social motivation. Dev Psychobiol 2008;50:322331.CrossRefGoogle ScholarPubMed
21.Burgdorf, J, Panksepp, J, Brudzynski, SMet al. The effects of selective breeding for differential rates of 50-kHz ultrasonic vocalizations on emotional behavior in rats. Dev Psychobiol 2009;51:3446.CrossRefGoogle ScholarPubMed
22.Mu, P, Fuchs, T, Saal, DB, Sorg, BA, Dong, Y, Panksepp, J. Repeated cocaine exposure induces sensitization of ultrasonic vocalization in rats. Neurosci Lett 2009;453:3135.CrossRefGoogle ScholarPubMed
23.Hofer, MA, Masmela, JR, Brunelli, SA, Shair, HN. The ontogeny of maternal potentiation of the infant rats’ isolation call. Dev Psychobiol 1998;33:189201.3.0.CO;2-N>CrossRefGoogle ScholarPubMed
24.Shair, HN, Masmela, JR, Brunelli, SA, Hofer, MA. Potentiation and inhibition of ultrasonic vocalization of rat pups: regulation by social cues. Dev Psychobiol 1997;30:195200.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
25.Hofer, MA, Brunelli, SA, Masmela, J, Shair, HN. Maternal interactions prior to separation potentiate isolation-induced calling in rat pups. Behav Neurosci 1996;110:11581167.CrossRefGoogle ScholarPubMed
26.Hofer, MA, Brunelli, SA, Shair, HN. Potentiation of isolation-induced vocalization by brief exposure of rat pups to maternal cues. Dev Psychobiol 1994;27:503517.CrossRefGoogle ScholarPubMed
27.Oswalt, GL, Meier, GW. Olfactory, thermal, and tactual influences on infantile ultrasonic vocalization in rats. Dev Psychobiol 1975;8:129135.CrossRefGoogle ScholarPubMed
28.Branchi, I, Santucci, D, Vitale, A, Alleva, E. Ultrasonic vocalizations by infant laboratory mice: a preliminary spectrographic characterization under different conditions. Dev Psychobiol 1998;33:249256.3.0.CO;2-R>CrossRefGoogle ScholarPubMed
29.Conely, L, Bell, RW. Neonatal ultrasounds elicited by odor cues. Dev Psychobiol 1978;11:193197.CrossRefGoogle ScholarPubMed
30.Hofer, MA, Shair, HN. Independence of ultrasonic vocalization and thermogenic responses in infant rats. Behav Neurosci 1991;105:4148.CrossRefGoogle ScholarPubMed
31.Kraebel, KS, Brasser, SM, Campbell, JO, Spear, LP, Spear, NE. Developmental differences in temporal patterns and potentiation of isolation-induced ultrasonic vocalizations: influence of temperature variables. Dev Psychobiol 2002;40:147159.CrossRefGoogle ScholarPubMed
32.Wilcox, RR. New Statistical Procedures for the Social Sciences: Modern Solutions to Basic Problems. Hillsdale: Erlbaum, 1987.Google Scholar
33.Fuchs, T, Iacobucci, P, Mackinnon, KM, Panksepp, J. Infant-mother recognition in a social rodent (Octodon degus). J Comp Psychol 2010;124:166175.CrossRefGoogle Scholar
34.Panksepp, J, Deeskinazi, FG. Opiates and homing. J Comp Physiol Psychol 1980;94:650663.CrossRefGoogle ScholarPubMed
35.Wiener, SG, Bayart, F, Faull, KF, Levine, S. Behavioral and physiological responses to maternal separation in squirrel monkeys (Saimiri sciureus). Behav Neurosci 1990;104:108115.CrossRefGoogle ScholarPubMed
36.Iacobucci, P, Colonnello, V, Newberry, RC. Piglets call for mother's attention: Piglet attachment vocal responses are modulated by proximity to their mother. Proceedings of the 41st Annual Meeting of the International Society for Developmental Psychobiology; 12–15 November 2008, Washington DC, USA.Google Scholar
37.Colonnello, V, Iacobucci, P, Panksepp, J. Analysis of the disruption of maternal social bonds in Octodon degus: separation distress in restricted reunion tests. Dev Psychobiol 2011;53:657669.CrossRefGoogle ScholarPubMed
38.Panksepp, J, Newman, JD, Insel, TR. Critical conceptual issues in the analysis of separation distress systems of the brain. In: Strongman KT, editor. International Review of Studies on Emotion, Vol. 2. USA: John Wiley & Sons, 1992.Google Scholar
39.Brunelli, SA, Keating, CC, Hamilton, NA, Hofer, MA. Development of ultrasonic vocalization responses in genetically heterogeneous National Institute of Health (N:NIH) rats. I. Influence of age, testing experience and associated factors. Dev Psychobiol 1996;29:507516.3.0.CO;2-Q>CrossRefGoogle Scholar
40.Brunelli, SA. Development and evolution of hidden regulators: selective breeding for an infantile phenotype. Dev Psychobiol 2005;47:243252.CrossRefGoogle ScholarPubMed
41.Forbes, EE, Dahl, RE. Neural systems of positive affect: relevance to understanding child and adolescent depression? Dev Psychopathol 2005;17:827850.CrossRefGoogle ScholarPubMed
42.Stelmack, RM. ed. On the Psychobiology of Personality: Essays in Honor of Marvin Zuckerman. Amsterdam: Elsevier Science, 2004.Google Scholar
43.Zuckerman, M. Psychobiology of Personality, 2nd edn. New York: Cambridge University Press, 2005.CrossRefGoogle Scholar
44.Lonigan, CJ, Phillips, BM, Hooe, ES. Relations of positive and negative affectivity to anxiety and depression in children: evidence from a latent variable longitudinal study. J Consult Clin Psychol 2003;71:465481.CrossRefGoogle ScholarPubMed