Variability in empathic fear response among 11 inbred strains of mice

Genes, Brain and Behavior

Volumn 15, Issue 2, 2016, Pages 231-242

  Keum, S ^a   Park, J ^a,b,c   Kim, A ^a   Kim, K K ^a   Jeong, J ^b   Shin, H S ^a  

^a Institute for Basic Science   (South Korea)

^b Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^c Korea Institute of Science and Technology   (South Korea)

Author keywords

Anxiety; Conditioned fear; Empathy; Genetic variability; Inbred mouse strain; Locomotion; Observational fear learning; Rodent model of empathic fear; Sex and age; Sociability; Social novelty preference

Indexed keywords

ADOLESCENT; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; ELEVATED PLUS MAZE TEST; EMPATHIC FEAR; EMPATHY; FEAR; FEAR CONDITIONING TEST; FEMALE; FOOTSHOCK; FREEZING; GENETIC REGULATION; GENETIC VARIABILITY; HIPPOCAMPUS; INBRED MOUSE STRAIN; LOCOMOTION; MALE; MOUSE; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; SEX DIFFERENCE; SOCIAL ADAPTATION; SOCIAL BEHAVIOR; STRAIN DIFFERENCE; ANIMAL; ANIMAL BEHAVIOR; CONDITIONED REFLEX; GENETICS; LEARNING; MEMORY; MOTOR ACTIVITY; PHYSIOLOGY; SPECIES DIFFERENCE;

ANIMALS; BEHAVIOR, ANIMAL; CONDITIONING, CLASSICAL; EMPATHY; FEAR; LEARNING; MALE; MEMORY; MICE; MOTOR ACTIVITY; SPECIES SPECIFICITY;

EID: 84956760688     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/gbb.12278     Document Type: Article

References (51)

1. Adriani, W. & Laviola, G. (2004) Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model. Behav Pharmacol 15, 341-352.
2. Atsak, P., Orre, M., Bakker, P., Cerliani, L., Roozendaal, B., Gazzola, V., Moita, M. & Keysers, C. (2011) Experience modulates vicarious freezing in rats: a model for empathy. PLoS ONE 6, e21855.
3. Balogh, S.A. & Wehner, J.M. (2003) Inbred mouse strain differences in the establishment of long-term fear memory. Behav Brain Res 140, 97-106.
4. Baran, S.E., Armstrong, C.E., Niren, D.C. & Conrad, C.D. (2010) Prefrontal cortex lesions and sex differences in fear extinction and perseveration. Learn Mem 17, 267-278.
5. Bernhardt, B.C. & Singer, T. (2012) The neural basis of empathy. Annu Rev Neurosci 35, 1-23.
6. Bird, G., Silani, G., Brindley, R., White, S., Frith, U. & Singer, T. (2010) Empathic brain responses in insula are modulated by levels of alexithymia but not autism. Brain 133, 1515-1525.
7. Bolivar, V.J., Pooler, O. & Flaherty, L. (2001) Inbred strain variation in contextual and cued fear conditioning behavior. Mamm Genome 12, 651-656.
8. Bora, E., Yucel, M. & Allen, N.B. (2009) Neurobiology of human affiliative behaviour: implications for psychiatric disorders. Curr Opin Psychiatry 22, 320-325.
9. Bothe, G.W., Bolivar, V.J., Vedder, M.J. & Geistfeld, J.G. (2005) Behavioral differences among fourteen inbred mouse strains commonly used as disease models. Comp Med 55, 326-334.
10. Brodkin, E.S. (2007) BALB/c mice: low sociability and other phenotypes that may be relevant to autism. Behav Brain Res 176, 53-65.
11. Brodkin, E.S., Hagemann, A., Nemetski, S.M. & Silver, L.M. (2004) Social approach-avoidance behavior of inbred mouse strains towards DBA/2 mice. Brain Res 1002, 151-157.
12. Brown, R.E. & Wong, A.A. (2007) The influence of visual ability on learning and memory performance in 13 strains of mice. Learn Mem 14, 134-144.
13. Chen, Q., Panksepp, J.B. & Lahvis, G.P. (2009) Empathy is moderated by genetic background in mice. PLoS ONE 4, e4387.
14. Crabbe, J.C., Wahlsten, D. & Dudek, B.C. (1999) Genetics of mouse behavior: interactions with laboratory environment. Science 284, 1670-1672.
15. Danziger, N., Faillenot, I. & Peyron, R. (2009) Can we share a pain we never felt? Neural correlates of empathy in patients with congenital insensitivity to pain. Neuron 61, 203-212.
16. Ebstein, R.P., Israel, S., Chew, S.H., Zhong, S. & Knafo, A. (2010) Genetics of human social behavior. Neuron 65, 831-844.
17. Fraser, L.M., Brown, R.E., Hussin, A., Fontana, M., Whittaker, A., O'Leary, T.P., Lederle, L., Holmes, A. & Ramos, A. (2010) Measuring anxiety- and locomotion-related behaviours in mice: a new way of using old tests. Psychopharmacology (Berl) 211, 99-112.
18. Frith, U. & Happe, F. (2005) Autism spectrum disorder. Curr Biol 15, R786-R790.
19. Gimenez, E. & Montoliu, L. (2001) A simple polymerase chain reaction assay for genotyping the retinal degeneration mutation (Pdeb(rd1)) in FVB/N-derived transgenic mice. Lab Anim 35, 153-156.
20. Golkar, A., Castro, V. & Olsson, A. (2015) Social learning of fear and safety is determined by the demonstrator's racial group. Biol Lett 11, 20140817.
21. Gonzalez-Liencres, C., Juckel, G., Tas, C., Friebe, A. & Brune, M. (2014) Emotional contagion in mice: the role of familiarity. Behav Brain Res 263, 16-21.
22. Hadjikhani, N., Zurcher, N.R., Rogier, O., Hippolyte, L., Lemonnier, E., Ruest, T., Ward, N., Lassalle, A., Gillberg, N., Billstedt, E., Helles, A., Gillberg, C., Solomon, P., Prkachin, K.M. & Gillberg, C. (2014) Emotional contagion for pain is intact in autism spectrum disorders. Transl Psychiatry 4, e343.
23. Hefner, K. & Holmes, A. (2007) Ontogeny of fear-, anxiety- and depression-related behavior across adolescence in C57BL/6J mice. Behav Brain Res 176, 210-215.
24. Hefner, K., Whittle, N., Juhasz, J., Norcross, M., Karlsson, R.M., Saksida, L.M., Bussey, T.J., Singewald, N. & Holmes, A. (2008) Impaired fear extinction learning and cortico-amygdala circuit abnormalities in a common genetic mouse strain. J Neurosci 28, 8074-8085.
25. Hovatta, I., Tennant, R.S., Helton, R., Marr, R.A., Singer, O., Redwine, J.M., Ellison, J.A., Schadt, E.E., Verma, I.M., Lockhart, D.J. & Barlow, C. (2005) Glyoxalase 1 and glutathione reductase 1 regulate anxiety in mice. Nature 438, 662-666.
26. Jeon, D., Kim, S., Chetana, M., Jo, D., Ruley, H.E., Lin, S.Y., Rabah, D., Kinet, J.P. & Shin, H.S. (2010) Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC. Nat Neurosci 13, 482-488.
27. Jeon, D. & Shin, H.S. (2011) A mouse model for observational fear learning and the empathetic response. In Crawley J. N., et al. (eds), Current Protocols in Neuroscience/Editorial Board, Chapter 8, Unit 8 27.
28. Keane, T.M., Goodstadt, L., Danecek, P. et al. (2011) Mouse genomic variation and its effect on phenotypes and gene regulation. Nature 477, 289-294.
29. Kulesskaya, N., Karpova, N.N., Ma, L., Tian, L. & Voikar, V. (2014) Mixed housing with DBA/2 mice induces stress in C57BL/6 mice: implications for interventions based on social enrichment. Front Behav Neurosci 8, 257.
30. Langford, D.J., Crager, S.E., Shehzad, Z., Smith, S.B., Sotocinal, S.G., Levenstadt, J.S., Chanda, M.L., Levitin, D.J. & Mogil, J.S. (2006) Social modulation of pain as evidence for empathy in mice. Science 312, 1967-1970.
31. Lee, K.H., Farrow, T.F., Spence, S.A. & Woodruff, P.W. (2004) Social cognition, brain networks and schizophrenia. Psychol Med 34, 391-400.
32. Lombardo, M.V., Barnes, J.L., Wheelwright, S.J. & Baron-Cohen, S. (2007) Self-referential cognition and empathy in autism. PLoS ONE 2, e883.
33. Miller, B.H., Schultz, L.E., Gulati, A., Su, A.I. & Pletcher, M.T. (2010) Phenotypic characterization of a genetically diverse panel of mice for behavioral despair and anxiety. PLoS ONE 5, e14458.
34. Minio-Paluello, I., Baron-Cohen, S., Avenanti, A., Walsh, V. & Aglioti, S.M. (2009) Absence of embodied empathy during pain observation in Asperger syndrome. Biol Psychiatry 65, 55-62.
35. Moy, S.S., Nadler, J.J., Young, N.B., Nonneman, R.J., Segall, S.K., Andrade, G.M., Crawley, J.N. & Magnuson, T.R. (2008) Social approach and repetitive behavior in eleven inbred mouse strains. Behav Brain Res 191, 118-129.
36. Moy, S.S., Nadler, J.J., Young, N.B., Perez, A., Holloway, L.P., Barbaro, R.P., Barbaro, J.R., Wilson, L.M., Threadgill, D.W., Lauder, J.M., Magnuson, T.R. & Crawley, J.N. (2007) Mouse behavioral tasks relevant to autism: phenotypes of 10 inbred strains. Behav Brain Res 176, 4-20.
37. Owen, E.H., Logue, S.F., Rasmussen, D.L. & Wehner, J.M. (1997) Assessment of learning by the Morris water task and fear conditioning in inbred mouse strains and F1 hybrids: implications of genetic background for single gene mutations and quantitative trait loci analyses. Neuroscience 80, 1087-1099.
38. Panksepp, J.B. & Lahvis, G.P. (2011) Rodent empathy and affective neuroscience. Neurosci Biobehav Rev 35, 1864-1875.
39. Paylor, R., Spencer, C.M., Yuva-Paylor, L.A. & Pieke-Dahl, S. (2006) The use of behavioral test batteries, II: effect of test interval. Physiol Behav 87, 95-102.
40. Pittler, S.J. & Baehr, W. (1991) Identification of a nonsense mutation in the rod photoreceptor cGMP phosphodiesterase beta-subunit gene of the rd mouse. Proc Natl Acad Sci USA 88, 8322-8326.
41. Sanders, D.S., Karajeh, M.A. & Hurlstone, D.P. (2005) Empathy, empowerment, political will and a coeliac specialist dietitian in every hospital? J Hum Nutr Diet 18, 467-468.
42. Schulte-Ruther, M., Markowitsch, H.J., Shah, N.J., Fink, G.R. & Piefke, M. (2008) Gender differences in brain networks supporting empathy. Neuroimage 42, 393-403.
43. Silverman, J.L., Yang, M., Lord, C. & Crawley, J.N. (2010) Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci 11, 490-502.
44. Singer, T., Seymour, B., O'Doherty, J., Kaube, H., Dolan, R.J. & Frith, C.D. (2004) Empathy for pain involves the affective but not sensory components of pain. Science 303, 1157-1162.
45. Singer, T., Seymour, B., O'Doherty, J.P., Stephan, K.E., Dolan, R.J. & Frith, C.D. (2006) Empathic neural responses are modulated by the perceived fairness of others. Nature 439, 466-469.
46. Voikar, V., Vasar, E. & Rauvala, H. (2004) Behavioral alterations induced by repeated testing in C57BL/6J and 129S2/Sv mice: implications for phenotyping screens. Genes Brain Behav 3, 27-38.
47. Wahlsten, D., Bachmanov, A., Finn, D.A. & Crabbe, J.C. (2006) Stability of inbred mouse strain differences in behavior and brain size between laboratories and across decades. Proc Natl Acad Sci USA 103, 16364-16369.
48. Wahlsten, D., Metten, P. & Crabbe, J.C. (2003) A rating scale for wildness and ease of handling laboratory mice: results for 21 inbred strains tested in two laboratories. Genes Brain Behav 2, 71-79.
49. Watanabe, S. (2011) Empathy and reversed empathy of stress in mice. PLoS ONE 6, e23357.
50. Wiesenfeld-Hallin, Z. (2005) Sex differences in pain perception. Gend Med 2, 137-145.
51. Yang, M., Abrams, D.N., Zhang, J.Y., Weber, M.D., Katz, A.M., Clarke, A.M., Silverman, J.L. & Crawley, J.N. (2012) Low sociability in BTBR T+tf/J mice is independent of partner strain. Physiol Behav 107, 649-662.