Scoring of Social Interactions and Play in Mice During Adolescence

M. Livia Terranova1, Giovanni Laviola1

1 Istituto Superiore di Sanità, Rome
Publication Name:  Current Protocols in Toxicology
Unit Number:  Unit 13.10
DOI:  10.1002/0471140856.tx1310s26
Online Posting Date:  December, 2005
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This unit provides a description of methods that have proven useful in characterizing amicable and playful interactions of developing mice. Such a procedure can be used to evaluate the effects of perinatal and/or ongoing treatments on the social performance of periadolescent subjects of either or both sexes. It can also be complemented by the use of specific acute drug challenges, which can throw light on possible alterations of the subserving neurochemical systems. Basically, it consists of video recording brief sessions of spontaneous pair interactions and their subsequent observation and scoring according to a detailed mouse ethogram. The protocol is quite sensitive to subtle behavioral effects, which could be undetectable by other means, and it is most useful when repeated over several days to draw an ontogenetic profile. Critical parameters that must be considered when planning, e.g., sample size and timing of observations, are discussed in detail, along with the key issue of controlling for litter effects.

Keywords: Behavior; Ontogeny; Affiliation; Critical periods; Rodents

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Table of Contents

  • Strategic Planning
  • Basic Protocol 1: Video Recording of Social Encounters
  • Basic Protocol 2: Observational Assessments
  • Commentary
  • Literature Cited
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Basic Protocol 1: Video Recording of Social Encounters

  • Periadolescent mice (from 21 to 45 postnatal days)
  • Isolated, soundproof experimental room equipped with red lights
  • Observation cages (standard housing cages with tops)
  • Standard sawdust
  • 2 to 3 small movable objects (e.g., food pellets)
  • Infrared video cameras, video recorders, monitors, and tapes
  • Event recorder system feeding to a computer with appropriate software
  • Balance for weighing animals
  • Nontoxic marker for subject identification
  • Paper labels for code identification
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Literature Cited

Literature Cited
   Adriani, W. and Laviola, G. 2000. A unique hormonal and behavioral hyporesponsivity to both forced novelty and D‐amphetamine in periadolescent mice. Neuropharmacology 39:334‐346.
   Adriani, W. and Laviola G. 2003. Elevated levels of impulsivity and reduced place conditioning with D‐amphetamine: Two behavioral features of adolescence in mice. Behav. Neurosci. 117:695‐703.
   Adriani, W., Chiarotti F., and Laviola G. 1998. Elevated novelty seeking and peculiar D‐amphetamine sensitization in periadolescent mice compared with adult mice. Behav. Neurosci. 112:1152‐1166.
   Adriani, W., Giannakopoulou, D., Bokulic, Z., Jerney, B., Alleva, E., and Laviola, G. 2005. Response to novelty, social and self‐control behaviors in rats exposed to neonatal anoxia: Modulatory effects of an enriched environment. Psychopharmacology. In press.
   Alleva, E. 1993. Assessment of aggressive behavior in rodents. Meth. Neurosci. 14:111‐137.
   Altmann, J. 1974. Observational study of behaviour: Sampling methods. Behaviour 49:227‐265.
   Chiarotti, F. and Sparks, T. 2002. Problems of data analysis in behavioural ecotoxicology. In Behavioural Ecotoxicology (G. Dell'Omo, ed.) pp. 273‐289. John Wiley & Sons, Hoboken, N.J.
   Chiarotti, F., Alleva, E., and Bignami, G. 1987. Problems of test choice and data analysis in behavioural teratology: The case of prenatal benzodiazepines. Neurobehav. Toxicol. Teratol. 9:179‐186.
   Cirulli, F., Bonsignore, L.T., Venerosi, A., and Valanzano, A. 2003. Long‐term effects of acute perinatal asphyxia on rat maternal behavior. Neurotoxicol. Teratol. 25:571‐578.
   Costa, L.G., Cole, T.B., and Furlong, C.E. 2003. Polymorphisms of paraoxonase (PON1) and their significance in clinical toxicology of organophosphates. J. Toxicol. Clin. Toxicol. 41:37‐45.
   Dixon, A.K., Fish, H.U., and McAllister, K.H. 1990. Ethopharmacology: A biological approach to the study of drug‐induced changes in behavior. Adv. Study Behav. 19:171‐204.
   Dyer, D.P. and Southwick, C.H. 1974. A possible sensitive period for juvenile socialization in mice. Behav. Biol. 12:551‐558.
   Einon, D.F., Humphreys, A.P., and Chivers, S.M. 1981. Isolation has permanent effects upon the behavior of the rat, but not the mouse, gerbil, or guinea pig. Develop. Psychobiol. 14:343‐355.
  File, S.E. and Hyde, J.R.G. 1978. Can social interaction be used to measure anxiety? Brit. J. Pharmacol. 62:19‐24.
   Grant, E.C. and Mackintosh, J.H. 1963. A comparison of the social postures of some common laboratory rodents. Behaviour 21:246‐259.
   Laviola, G. and Alleva, E. 1995. Sibling effects on the behaviour of infant mouse litters (Mus domesticus). J. Comp. Psychol. 109:68‐75.
   Laviola, G., Terranova, M.L., Sedowofia, K., Clayton, R., and Manning, A. 1993. A mouse model of early social interaction after prenatal drug exposure: A genetic investigation. Psychopharmacology 113:388‐394.
   Laviola, G., Macri, S., Morley‐Fletcher, S., and Adriani, W. 2003. Risk‐taking behavior in adolescent mice: Psychobiological determinants and early epigenetic influence. Neurosci. Biobehav. Rev. 27:19‐31.
   Laviola, G., Rea, M., Morley‐Fletcher, S., Di Carlo, S., Bacosi, A., De Simone, R., Bertini, M., and Pacifici, R. 2004a. Beneficial effects of enriched environment on adolescent rats from stressed pregnancies. Eur. J. Neurosci. 20:1655‐1664.
  Laviola, G., Adriani, W., Rea, M., Aloe, L., and Alleva, E. 2004b. Social withdrawal, neophobia, and stereotyped behavior in developing rats exposed to neonatal asphyxia. Psychopharmacology. 175:196‐205.
   Lore, R. and Flannelly, W. 1977. Rat societies. Sci. Amer. 236:106‐118.
   Mackintosh, J.H. 1981. Behaviour of the house mouse. In Biology of the House Mouse, Symp. Zool. Soc. Lond., vol. 47 (R.J. Berry, ed.) pp. 337‐365. Academic Press, London.
   Martin, P. and Bateson, P. 1986. Measuring Behaviour: An Introductory Guide. Cambridge University Press, Cambridge.
   Martin, P. and Caro, T.M. 1985. On the functions of play and its role in behavioral development. Adv. Study Behav. 15:59‐103.
   Meaney, M.J. and Stewart, J. 1981. A descriptive study of social development in the rat (Rattus norvegicus). Anim. Behav. 29:34‐45.
   Monroe, B.D. and Milner, J.S. 1977. Social deprivation and novelty effects on gregarious behavior in the rat. Bull. Psychon. Soc. 9:219‐220.
   Nadler, J.J., Moy, S.S., Dold, G., Trang, D., Simmons, N., Perez, A., Young, N.B., Barbaro, R.P., Piven, J., Magnuson, T.R., and Crawley, J.N. 2004. Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav. 3:303‐314.
   Palanza, P., Morellini, F., Parmigiani, S., and vom Saal, F.S. 2002. Ethological methods to study the effects of maternal exposure to estrogenic endocrine disrupters: A study with methoxychlor. Neurotoxicol. Teratol. 24:55‐69.
   Panksepp, J. and Beatty, W.W. 1980. Social deprivation and play in rats. Behav. Neur. Biol. 30:197‐206.
   Panksepp, J., Sivij, S., and Normansell, L. 1984. The psychobiology of play: Theoretical and methodological perspectives. Neurosci. Biobehav. Rev. 8:465‐492.
   Pellis, S.M., Pellis, V.C., Manning, C.J., and Dewsbury, D.A. 1991. The paucity of social play in juvenile Mus domesticus: What is missing from the behavioural repertoire? Anim. Behav. 42:686‐687.
   Poole, T.B. and Fish, J. 1975. An investigation of playful behaviour in Rattus norvegicus and Mus musculus (Mammalia). J. Zool. Soc. (Lond.) 175:61‐71.
   Primus, R.J. and Kellogg, C.K. 1989. Pubertal‐related changes influence the development of environment‐related social interaction in the male rat. Dev. Psychobiol. 22:633‐643.
   Puopolo, M., Vitale, A., and Laviola, G. (ed.) 2004. Biostatistical and ethological approaches for the promotion of welfare of laboratory animals and quality of experimental data. Ann. Ist. Super. Sanità 40:244.
   Ricceri, L., Markina, N., Valanzano, A., Fortuna, S., Cometa, M.F., Meneguz, A., and Calamandrei, G. 2003. Developmental exposure to chlorpyrifos alters reactivity to environmental and social cues in adolescent mice. Toxicol. Appl. Pharmacol. 191:189‐201.
   Santucci, D., Puopolo, M., Chiarotti, F., and Alleva, E. 1998. Neurobehavioural endpoints of endocrine disrupters in laboratory rodents: Methodological and regulatory (test guidelines) issues. UBA Texte 50:114‐128.
   Smith, E.S.F. 1991. The influence of nutrition and postpartum mating on weaning and subsequent play behaviour of hooded rats. Anim. Behav. 41:513‐524.
   Spear, L. and Brake, S.C. 1983. Periadolescence: Age‐dependent behavior and psychopharmacological responsivity in rats. Develop. Psychobiol. 16:83‐109.
   Terranova, M.L. and Laviola, G. 1995. Individual differences in mouse behavioural development: Effects of precocious weaning and ongoing sexual segregation. Anim. Behav. 50:1261‐1271.
   Terranova, M.L. and Laviola, G. 2001. δ‐opioid modulation of social interactions in juvenile mice weaned at different ages. Physiol. Behav. 73:393‐400.
   Terranova, M.L., Laviola, G., and Alleva, E. 1993. Ontogeny of amicable social behaviour in the mouse: Gender differences and on‐going isolation outcomes. Develop. Psychobiol. 26:467‐481.
   Thor, W.H. and Holloway, D.R. 1984. Sex and social play in juvenile rats (Rattus norvegicus). J. Comp. Psychol. 98:376‐384.
   Thor, W.H. and Holloway, D.R. 1986. Social play soliciting by male and female juvenile rats: Effects of neonatal androgenization and sex of cagemates. Behav. Neurosci. 100:275‐279.
   Van Oortmerssen, G.A. 1971. Biological significance, genetics and evolutionary origin of variability in behaviour within and between inbred strains of mice (Mus musculus), a behaviour genetic study. Behaviour 38:1‐92.
   Venerosi, A., Cirulli, F., Capone, F., and Alleva, E. 2003. Prolonged perinatal AZT administration and early maternal separation: Effects on social and emotional behaviour of periadolescent mice. Pharmacol. Biochem. Behav. 74:671‐681.
   Walker, C. and Byers, J.A. 1991. Heritability of locomotor play in house mice, Mus domesticus. Anim. Behav. 42:891‐897.
   Williams, E. and Scott, J.P. 1953. The development of social behaviour patterns in the mouse, in relation to natural periods. Behaviour 6:35‐65.
   Wills, G.D., Wesley, A.L., Moore, F.R., and Sisemore, D.A. 1983. Social interactions among rodent conspecifics: A review of the experimental paradigms. Neurosci. Biobehav. Rev. 7:315‐323.
   Wolff, R.J. 1981. Solitary and social play in wild Mus musculus (Mammalia). J. Zool. (Lond.) 195:405‐412.
   Zorrilla, E.P. 1997. Multiparous species present problems (and possibilities) to developmentalists. Dev. Psychobiol. 30:141‐150.
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