Relationships of open-field behaviour with anxiety in the elevated zero-maze test: Focus on freezing and grooming

Abstract

The National Institutes of Health Genetically Heterogeneous Rat Stock (NIH-HS) is a unique tool for genetic studies of complex traits due to its high genetic heterogeneity and to its high level of genetic recombinants accumulated along many outbreeding generations. In the present study, 90 NIH-HS male rats were tested for anxiety/fearfulness in the elevated zero-maze and in the open-field test in order to investigate the associations among defensive responses from both tests and, in particular, those among open- field self-grooming and freezing. These associations were evaluated by means of a correlational-factorial approach and an analysis of differences between sub- groups displaying extreme scores in representative variables. The final factor analysis revealed a first factor with high loadings of all variables from the zero-maze (“Maze timidity/conflict” factor), and a second (independent) factor dominated by open-field crossings (-0.74), rearings (-0.62) and freezing (0.65), with lower loadings of open-field grooming (-0.39) and stretched attend postures, as well as of entries and time (loadings of -0.32 to -0.25) in the open sections of the zero-maze (“Open Behavior inhibition/ desinhibition” factor), suggesting that open-field self-grooming is a response associated to activity, in the present study, rather than to inhibition. Furthermore, the finding that grooming in the OF loaded negatively in a second factor supports a relationship between grooming and dearousal. Present results, thus, are in accordance with the usefulness of these tests for the purposes they are commonly employed and add new evidence supporting their concurrent validity, as indicated by the relationships observed among measures from both tests.

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Díaz-Morán, S. , Estanislau, C. , Cañete, T. , Blázquez, G. , Ráez, A. , Tobeña, A. and Fernández-Teruel, A. (2014) Relationships of open-field behaviour with anxiety in the elevated zero-maze test: Focus on freezing and grooming. World Journal of Neuroscience, 4, 1-11. doi: 10.4236/wjns.2014.41001.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Hansen, C. and Spuhler, K. (1984) Development of the National Institutes of Health genetically heterogeneous stock. Alcoholism: Clinical and Experimental Research, 8, 477-479. http://dx.doi.org/10.1111/j.1530-0277.1984.tb05706.x
[2] Spuhler, K. and Dietrich, R.A. (1984) Correlative analysis of ethanol-related phenotypes in rat inbred strains. Alcoholism: Clinical and Experimental Research, 8, 480-484.
http://dx.doi.org/10.1111/j.1530-0277.1984.tb05707.x
[3] Baud, A., Hermsen, R., Guryev, V., Stridh, P., Graham, D., McBride, M.W., et al., (2013) Combined sequencebased and genetic mapping analysis of complex traits in outbred rats. Nature Genetics, 45, 767-775.
http://dx.doi.org/10.1038/ng.2644
[4] Díaz-Morán, S., Mont-Cardona, C., Canete, T., Blázquez, G., Martínez-Membrives, E., López-Aumatell, R., Tobena, A. and Fernández-Teruel, A. (2012) Coping style and stress hormone responses in genetically heterogeneous rats: Comparison with the Roman rat strains. Behavioural Brain Research, 228, 203-210.
http://dx.doi.org/10.1016/j.bbr.2011.12.002?
[5] Díaz-Morán, S., Martínez-Membrives, E., López-Aumatell, R., Canete, T., Blázquez, G., Palencia, M., Mont-Cardona, C., Estanislau, C., Tobena, A. and Fernández-Teruel, A. (2013) What can we learn on rodent fearfulness/ anxiety from the genetically heterogeneous NIH-HS rat stock? Open Journal of Psychiatry, 3, 238-250.
http://dx.doi.org/10.4236/ojpsych.2013.32022
[6] Johannesson, M., López-Aumatell, R., Stridh, P., Diez, M., Tuncel, J., Blázquez, G., et al. (2009) A resource for the simultaneous high-resolution mapping of multiple quantitative trait loci in rats: The NIH heterogeneous stock. Genome Research, 19, 150-158.
http://dx.doi.org/10.1101/gr.081497.108
[7] López-Aumatell, R., Guitart-Masip, M., Vicens-Costa, E., Giménez-Llort, L., Valdar, W., Johannesson, M., Flint, J. Tobena, A. and Fernandez-Teruel, A. (2008) Fearfulness in a large N/Nih genetically heterogeneous rat stock: Differential profiles of timidity and defensive flight in males and females. Behavioural Brain Research, 188, 41-55. http://dx.doi.org/10.1016/j.bbr.2007.10.015?
[8] López-Aumatell, R., Vicens-Costa, E., Guitart-Masip, M., Martínez-Membrives, E., Valdar, W., Johannesson, M., Canete, T., Blázquez, G., Driscoll, P., Flint, J., Tobena, A. and Fernández-Teruel, A. (2009) Unlearned anxiety predicts learned fear: A comparison among heterogeneous rats and the Roman rat strains. Behavioural Brain Research, 202, 92-101.
http://dx.doi.org/10.1016/j.bbr.2009.03.024
[9] López-Aumatell, R., Martínez-Membrives, E., VicensCosta, E., Canete, T., Blázquez, G., Mont-Cardona, C., Johannesson, M., Flint, J., Tobena A. and Fernández-Teruel, A. (2011) Effects of environmental and physiological covariates on sex differences in unconditioned and conditioned anxiety and fear in a large sample of genetically heterogeneous (N/Nih-HS) rats. Behavioral and Brain Functions, 7, 48.
http://dx.doi.org/10.1186/1744-9081-7-48
[10] Palència, M., Díaz-Morán, S., Mont-Cardona, C., Canete, T., Blázquez, G., Martínez-Membrives, E., López-Aumatell, R., Tobena, A. and Fernández-Teruel, A. (2013) Helplessness-like escape deficits of NIH-HS rats predict passive behavior in the forced swimming test: Relevance for the concurrent validity of rat models of depression. World Journal of Neuroscience, 3, 83-92.
http://dx.doi.org/10.4236/wjns.2013.32012
[11] Vicens-Costa, E., Martínez-Membrives, E., López-Aumatell, R., Guitart-Masip, M., Canete, T., Blázquez, G., Tobena, A. and Fernández-Teruel, A. (2011) Two-way avoidance acquisition is negatively related to conditioned freezing and positively associated with startle reactions: A dissection of anxiety and fear in genetically heterogeneous rats. Physiology & Behavior, 103, 148-156.
http://dx.doi.org/10.1016/j.physbeh.2010.12.009?
[12] Broadhurst, P.L. (1957) Determinants of emotionality in the rat. I. Situational factors. British Journal of Psychology, 48, 1-12.
http://dx.doi.org/10.1111/j.2044-8295.1957.tb00594.x
[13] Broadhurst, P.L. (1958) Determinants of emotionality in the rat. II. Antecedent factors. British Journal of Psychology, 49, 12-20.
http://dx.doi.org/10.1111/j.2044-8295.1958.tb00632.x
[14] Broadhurst, P.L. (1975) The Maudsley reactive and non reactive strains of rats: A survey. Behavior Genetics, 5, 299-319. http://dx.doi.org/10.1007/BF01073201
[15] Escorihuela, R.M., Fernández-Teruel, A., Gil, L., Aguilar, R., Tobena, A. and Driscoll, P. (1999) Inbred Roman highand low-avoidance rats: Differences in anxiety, novelty-seeking, and shuttlebox behaviors. Physiology & Behavior, 67, 19-26.
http://dx.doi.org/10.1016/S0031-9384(99)00064-5
[16] Escorihuela, R.M. and Fernández-Teruel, A. (1998) Modelos animales en psicopatologia y psicofarmacologia: Del análisis experimental de la conducta a la neurogenética. Psicología conductista, 6, 165-191.
[17] Fernandez-Teruel, A., Escorihuela, R.M., Nunez, J.F., Gomá, M., Driscoll, P. and Tobena, A. (1992) Early stimulation effects on novelty-induced behavior in two psychogenetically-selected rat lines with divergent emotionality profiles. Neuroscience Letters, 137, 185-188.
http://dx.doi.org/10.1016/0304-3940(92)90400-2
[18] Gray, J.A. and Lalljee, B. (1974) Sex differences in emotional behavior in the rat: Correlation between open field defecation and active avoidance. Animal Behaviour, 22, 856-861.
http://dx.doi.org/10.1016/0003-3472(74)90008-6
[19] Gray, J.A. and McNaughton, N. (2000) The neuropsychology of anxiety: An enquiry into the functions of the septo-hippocampal system. Oxford University Press, Oxford.
[20] Levine, S. and Broadhurst, P.L. (1963) Genetic and ontogenetic determinants of adult behavior in the rat. Journal of Comparative and Physiological Psychology, 56, 423-428.
http://dx.doi.org/10.1037/h0040285
[21] [Aguilar, R., Gil, L., Flint, J., Gray, J.A., Dawson, G.R., Driscoll, P., et al., (2002) Learned fear, emotional reactivity and fear of heights: A factor analytic map from a large F2 intercross of Roman rat strains. Brain Research Bulletin, 57, 17-26.
[22] Aguilar, R., Gil, L., Gray, J.A., Driscoll, P., Flint, J., Dawson, G.R., Giménez-Llort, L., Escorihuela, R.M., Fernández-Teruel, A. and Tobena, A. (2003) Fearfulness and sex in F2 Roman rats: Males display more fear though both sexes share the same fearfulness traits. Physiology & Behavior, 78, 723-732.
http://dx.doi.org/10.1016/S0031-9384(03)00043-X
[23] Steimer, T. and 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, 6, 87-100.
http://dx.doi.org/10.1080/1025389031000111320
[24] Steimer, T., Escorihuela, R.M., Fernández-Teruel, A. and Driscoll, P. (1998) Long-term behavioural and neuroendocrine changes in Roman high-(RHA/Verh) and low(RLA-Verh) avoidance rats following neonatal handling. International Journal of Developmental Neuroscience, 16, 165-174.
http://dx.doi.org/10.1016/S0736-5748(98)00032-X
[25] Ferré, P., Fernández-Teruel, A., Escorihuela, R.M., Driscoll, P., Corda, M.G., Giorgi, O. and Tobena, A. (1995) Behavior of the Roman/Verh highand low-avoidance rat lines in anxiety tests: Relationship with defecation and self-grooming. Physiology & Behavior, 58, 1209-1213.
http://dx.doi.org/10.1016/0031-9384(95)02068-3
[26] Spruijt, B.M., van Hooff, J.M. and Gispen, W.H. (1992) The ethology and neurobiology of grooming behavior. Physiological Reviews, 72, 825-852.
[27] Giorgi, O., Lecca, D., Piras, G., Driscoll, P. and Corda, M.G. (2003) Dissociation between mesocortical dopamine release and fear-related behaviours in two psychogenetically selected lines of rats that differ in coping strategies to aversive conditions. European Journal of Neuroscience, 17, 2716-2726.
http://dx.doi.org/10.1046/j.1460-9568.2003.02689.x
[28] Cruz, A.P.M., Frei, F. and Graeff, F.G. (1994) Ethopharmacological analysis of rat behavior on the elevated plus-maze. Pharmacology Biochemistry and Behavior, 49, 171-176.
http://dx.doi.org/10.1016/0091-3057(94)90472-3
[29] Anseloni, V.Z. and Brandno, M.L. (1997) Ethopharmacological analysis of behaviour of rats using variations of the elevated plus-maze. Behavioural Pharmacology, 8, 533-540.
http://dx.doi.org/10.1097/00008877-199711000-00011
[30] Prut, L. and Belzung, C. (2003) The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: A review. European Journal of Pharmacology, 463, 3-33.
http://dx.doi.org/10.1016/S0014-2999(03)01272-X
[31] Guitart-Masip, M., Giménez-Llort, L., Fernández-Teruel, A., Canete, T., Tobena, A., Ogren, S.O., Terenius, L. and Johansson, B. (2006) Reduced ethanol response in the alcohol-preferring RHA rats and neuropeptide mRNAs in relevant structures. European Journal of Neuroscience, 23, 531-540.
http://dx.doi.org/10.1016/S0014-2999(03)01272-X
[32] Pahkla, R., Kask, A. and Rago, L. (2000) Differential effects of beta-carbolines and antidepressants on rat exploratory activity in the elevated zero-maze. Pharmacology Biochemistry and Behavior, 65, 737-742.
http://dx.doi.org/10.1016/S0091-3057(99)00265-8
[33] Shepherd, J,K., Grewal, S.S., Fletcher, A., Bill, D.J. and Dourish, C.T. (1994) Behavioural and pharmacological characterisation of the elevated “zero-maze” as an animal model of anxiety. Psychopharmacol, 116, 56-64.
http://dx.doi.org/10.1007/BF02244871
[34] Bindra, D. and Spinner, N. (1958) Response to different degrees of novelty: The incidence of various activities. Journal of the Experimental Analysis of Behavior, 1, 341-350. http://dx.doi.org/10.1901/jeab.1958.1-341
[35] Fentress, J.C. (1968) Interrupted ongoing behavior in two species of vole (Microtus agrestis and Clethrionomys brittannicus) I: Response as a function of preceeding activity and the context of apparently irrelevant motor patterns. Animal Behaviour, 16, 135-153.
http://dx.doi.org/10.1016/0003-3472(68)90124-3
[36] Hannigan, J.H. and Issacson, R.L. (1981) Conditioned excessive grooming in the rat after footshock: Effect of naloxone and situational cues. Behavioral and Neural Biology, 33, 280-292.
http://dx.doi.org/10.1016/S0163-1047(81)92045-8
[37] Van Erp, A.M.M., Kruk, M.R., Meelis, W. and WillekensBramer, D.C. (1994) Effect of environmental stressors on time course, variability and form of self-grooming in the rat: Handling, social contact, defeat, novelty, restraint and fur moistening. Behavioural Brain Research, 65, 47-55.
http://dx.doi.org/10.1016/0166-4328(94)90072-8
[38] Bouwknecht, J.A., Spiga, F., Staub, D.R., Hale, M.W., Shekhar, A. and Lowry, C.A. (2007) Differential effects of exposure to low-light or high-light open-field on anxiety-related behaviors: Relationship to c-Fos expression in serotonergic and non-serotonergic neurons in the dorsal raphe nucleus. Brain Research Bulletin, 72, 32-43.
http://dx.doi.org/10.1016/j.brainresbull.2006.12.009
[39] Mairesse, J., Viltart, O., Salome, N., Giuliani, A., Catalani, A., Casolini, P., et al. (2007) Prenatal stress alters the negative correlation between neuronal activation in limbic regions and behavioral responses in rats exposed to high and low anxiogenic environments. Psychoneuroendocrinology, 32, 765-776.
http://dx.doi.org/10.1016/j.psyneuen.2007.03.013
[40] Estanislau, C. (2012) Cues to the usefulness of grooming behavior in the evaluation of anxiety in the elevated plus-maze. Psychology & Neuroscience, 5, 105-112.
http://dx.doi.org/10.3922/j.psns.2012.1.14
[41] Estanislau, C., Díaz-Morán, S., Canete, T., Blázquez, G., Tobena, A. and Fernández-Teruel, A. (2013) Contextdependent differences in grooming behavior among the NIH heterogeneous stock and the Roman highand lowavoidance rats. Neuroscience Research, 77, 187-201.
http://dx.doi.org/10.1016/j.neures.2013.09.012?
[42] Estanislau, C., Ramos, A.C., Ferraresi, P.D., Costa, N.F., de Carvalho, H.M.C.P. and Batistela, S. (2011) Individual differences in the elevated plus-maze and the forced swim test. Behavioural Processes, 86, 46-51.
http://dx.doi.org/10.1016/j.beproc.2010.08.008
[43] Kalueff, A.V. and Tuohimaa, P. (2005) The grooming analysis algorithm discriminates between different levels of anxiety in rats: Potential utility for neurobehavioural stress research. Journal of Neuroscience Methods, 143, 169-177.
http://dx.doi.org/10.1016/j.jneumeth.2004.10.001
[44] Komorowska, J. and Pisula, W. (2003) Does changing levels of stress affect the characteristics of grooming behavior in rats? International Journal of Comparative Psychology, 16, 237-246.

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