The role of behavior in translational models for psychopathology: Functionality and dysfunctional behaviors

Neuroscience and Biobehavioral Reviews

Volumn 37, Issue 8, 2013, Pages 1567-1577

  Blanchard, D Caroline ^a   Summers, Cliff H ^b,c   Blanchard, Robert J ^a,d  

^a Pacific Biosciences Research Center   (United States)

^b University of South Dakota   (United States)

^c UNIVERSITY OF SOUTH DAKOTA   (United States)

^d UNIVERSITY OF HAWAII   (United States)

Author keywords

Adaptive behavior; Animal models; Anxiety; Autism; Biomarkers; Depression; Functionality of behavior; Psychopathology; Translational research

Indexed keywords

AMPHETAMINE; BIOLOGICAL MARKER; DOPAMINE RECEPTOR STIMULATING AGENT; HEPARAN SULFATE;

ADAPTIVE BEHAVIOR; ANOREXIA; ANXIETY DISORDER; AUTISM; BEHAVIOR DISORDER; BRAIN FUNCTION; CONSTRUCT VALIDITY; DEFENSIVE BEHAVIOR; DEPRESSION; DRUG DEPENDENCE; ELECTROENCEPHALOGRAM; FACE VALIDITY; FACIAL EXPRESSION; FUNCTIONAL DISEASE; HUMAN; MEDICAL CARE; MENTAL DISEASE; NONHUMAN; OBSESSIVE COMPULSIVE DISORDER; PREDICTION; PRIORITY JOURNAL; REVIEW; SCHIZOPHRENIA; SOCIAL BEHAVIOR; SOCIAL ENVIRONMENT; UNITED STATES; VALIDITY;

ADAPTIVE BEHAVIOR; ANIMAL MODELS; ANXIETY; AUTISM; BIOMARKERS; DEPRESSION; FUNCTIONALITY OF BEHAVIOR; PSYCHOPATHOLOGY; TRANSLATIONAL RESEARCH;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; MENTAL DISORDERS; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84880031916     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2013.06.008     Document Type: Review

References (86)

1. Amara S.G., Grillner S., Insel T., Nutt D., Tsumoto T. Neuroscience in recession. Nature Reviews Neuroscience 2011, 12(5):297-302.
2. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders, DSM-IV-TR 2000, American Psychiatric Association, Washington, DC. 4th ed.
3. Arakawa H., Blanchard D.C., Blanchard R.J. Colony formation of C57BL/6J mice in visible burrow system: identification of eusocial behaviors in a background strain for genetic animal models of autism. Behavioural Brain Research 2007, 176(1):27-39.
4. Axelsson J., Xu D., Kang B.N., Nussbacher J.K., Handel T.M., Ley K., Sriramarao P., Esko J.D. Inactivation of heparan sulfate 2-O-sulfotransferase accentuates neutrophil infiltration during acute inflammation in mice. Blood 2012, 120(8):1742-1751.
5. Baird G., Cass H., Slonims V. Diagnosis of autism. British Medical Journal 2003, 327:488-493.
6. Benus R.F., Bohus B., Koolhaas J.M., van Oortmerssen G.A. Heritable variation for aggression as a reflection of individual coping strategies. Experientia 1991, 47(10):1008-1019.
7. Bitterman M.E. Toward a comparative psychology of learning. American Psychologist 1960, 15(11):704-712.
8. Blanchard D.C. Of lion manes and human beards: some unusual effects of the interaction between aggression and sociality. Frontiers in Behavioral Neuroscience 2010, 3:45.
9. Blanchard D.C., Blanchard R.J., Griebel G. Defensive responses to predator threat in the rat and mouse. Current Protocols in Neuroscience 2005, 1-2. (Chapter 8, Unit 8.19).
10. Blanchard D.C., Blanchard R.J., Lee E.M., Nakamura S. Defensive behaviors in rats following septal and septal - amygdala lesions. Journal of Comparative and Physiological Psychology 1979, 93(2):378-390.
11. Blanchard D.C., Hynd A.L., Minke K.A., Minemoto T., Blanchard R.J. Human defensive behaviors to threat scenarios show parallels to fear- and anxiety-related defense patterns of non-human mammals. Neuroscience and Biobehavioral Reviews 2001, 25(7-8):761-770.
12. Blanchard D.C., Defensor E.B., Meyza K.Z., Pobbe R.L., Pearson B.L., Bolivar V.J., Blanchard R.J. BTBR T+tf/J mice: autism-relevant behaviors and reduced fractone-associated heparan sulfate. Neuroscience and Biobehavioral Reviews 2012, 36(1):285-296.
13. Blanchard R.J., Blanchard D.C. Antipredator defensive behaviors in a visible burrow system. Journal of Comparative Psychology 1989, 103(1):70-82.
14. Blanchard R.J., Wall P.M., Blanchard D.C. Problems in the study of rodent aggression. Hormones and Behavior 2003, 44(3):161-170.
15. Brain P.F. Differentiating types of attack and defense in rodents. Multidisciplinary Approaches to Aggression Research 1979, 53-77. Elsevier, North Holland/Amsterdam. P.F. Brain, D. Benton (Eds.).
16. Budget of NASA, n.d. In Wikipedia. Retrieved from: http://en.wikipedia.org/wiki/Budget_of_NASA.
17. Calhoun J.B. Determinants of social organization exemplified in a single population of domesticated rats. Transactions of the New York Academy of Sciences 1961, 23:437-442.
18. Castagné V., Moser P., Roux S., Porsolt R.D. Rodent models of depression: forced swim and tail suspension behavioral despair tests in rats and mice. Current Protocols in Neuroscience 2011, (Chapter 8, Unit 8.10.A).
19. Chindo B.A., Adzu B., Yahaya T.A., Gamaniel K.S. Ketamine-enhanced immobility in forced swim test: a possible animal model for the negative symptoms of schizophrenia. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2012, 38(2):310-316.
20. Darwin C. On the Expression of Emotions in Man and Animals 1872, John Murray, London.
21. Defensor E.B., Corley M.J., Blanchard R.J., Blanchard D.C. Facial expressions of mice in aggressive and fearful contexts. Physiology and Behavior 2012, 107(5):680-685.
22. Defensor E.B., Pearson B.L., Pobbe R.L., Bolivar V.J., Blanchard D.C., Blanchard R.J. A novel social proximity test suggests patterns of social avoidance and gaze aversion-like behavior in BTBR T+tf/J mice. Behavioural Brain Research 2011, 217:302-308.
23. Ekman P. Universals and cultural differences in facial expression of emotion. Nebraska Symposium on Motivation 1972, 207-283. University of Nebraska Press, Lincoln, Nebraska. J. Cole (Ed.).
24. Estes R.D., Otte D., Wilson E.O. The Behavior Guide to African Mammals: Including Hoofed Mammals, Carnivores, Primates 1991, University of California Press, Berkeley, CA.
25. European Medical Research Councils (EMRC) White Paper: Present Status and Future Strategy for Medical Research in Europe 2007, 51 pp. European Science Foundation.
26. Gallo R.C. A reflection on HIV/AIDS research after 25 years. Retrovirology 2006, 3:72.
27. Geschwind D.H. Genetics of autism spectrum disorders. Trends in Cognitive Sciences 2011, 15:409-416.
28. Gray J.A. The neuropsychology of anxiety. British Journal of Psychology 1978, 69(4):417-434.
29. Groothuis T.G., Trillmich F. Unfolding personalities: the importance of studying ontogeny. Developmental Psychobiology 2011, 53(6):641-655.
30. Hendrie C., Pickles A. The failure of the antidepressant drug discovery process is systemic. Journal of Psychopharmacology 2012, (Epub ahead of print).
31. Hubbard D.T., Blanchard D.C., Yang M., Markham C.M., Gervacio A., Chun I.L., Blanchard R.J. Development of defensive behavior and conditioning to cat odor in the rat. Physiology and Behavior 2004, 80(4):525-530.
32. Hunt C., Peters L., Rapee R.M. Development of a measure of the experience of being bullied in youth. Psychological Assessment 2012, 24(1):156-165.
33. Irie F., Badie-Mahdavi H., Yamaguchi Y. Autism-like socio-communicative deficits and stereotypies in mice lacking heparan sulfate. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:5052-5056.
34. Kety S.S. Toward hypotheses for a biochemical component in the vulnerability to schizophrenia. Seminars in Psychiatry 1972, 4(3):233-238.
35. Kreuger J., Kjellén L. Heparan sulfate biosynthesis: regulation and variability. Journal of Histochemistry and Cytochemistry 2012, 60(12):898-907.
36. Kreuger J., Spillmann D., Li J.P., Lindahl U. Interactions between heparan sulfate and proteins: the concept of specificity. Journal of Cell Biology 2006, 174(3):323-327.
37. Landrigan P.J. What causes autism? Exploring the environmental contribution. Current Opinion in Pediatrics 2010, 22:219.
38. Langford D.J., Bailey A.L., Chanda M.L., Clarke S.E., Drummond T.E., Echols S., Glick S., Ingrao J., Klassen-Ross T., Lacroix-Fralish M.L., Matsumiya L., Sorge R.E., Sotocinal S.G., Tabaka J.M., Wong D., van den Maagdenberg A.M., Ferrari M.D., Craig K.D., Mogil J.S. Coding of facial expressions of pain in the laboratory mouse. Nature Methods 2010, 7(6):447-449.
39. Leyhausen P. Cat Behaviour: The Predatory and Social Behaviour of Domestic and Wild Cats 1979, STPM Press, New York.
40. Lord C.E. Autism: from research to practice. American Psychologist 2010, 65(8):815-826.
41. Markham C.M., Taylor S.L., Huhman K.L. Role of amygdala and hippocampus in the neural circuit subserving conditioned defeat in Syrian hamsters. Learning and Memory 2010, 17(2):109-116.
42. McFarlane H.G., Kusek G.K., Yang M., Phoenix J.L., Bolivar V.J., Crawley J.N. Autism-like behavioral phenotypes in BTBR T+tf/J mice. Genes, Brain and Behavior 2008, 7(2):152-163.
43. McMahon W.M., Baty B.J., Botkin J. Genetic counseling and ethical issues for autism. American Journal of Medical Genetics Part C 2006, 142C:52-57.
44. McKinney W.T., Bunney W.E. Animal model of depression. I. Review of evidence: implications for research. Archives of General Psychiatry 1969, 21(2):240-248.
45. McNaughton N., Corr P.J. A two-dimensional neuropsychology of defense: fear/anxiety and defensive distance. Neuroscience and Biobehavioral Reviews 2004, 28(3):285-305.
46. Meyer U., Feldon J. Epidemiology-driven neurodevelopmental animal models of schizophrenia. Progress in Neurobiology 2010, 90(3):285-326.
47. Meyza K.Z., Blanchard D.C., Pearson B.L., Pobbe R.L., Blanchard R.J. Fractone-associated N-sulfated heparan sulfate shows reduced quantity in BTBR T+tf/J mice: a strong model of autism. Behavioural Brain Research 2012, 228(2):247-253.
48. Mobbs D., Hassabis D., Seymour B., Marchant J.L., Weiskopf N., Dolan R.J., Frith C.D. Choking on the money: reward-based performance decrements are associated with midbrain activity. Psychological Science 2009, 20(8):955-962.
49. Moy S.S., Nadler J.J., Magnuson T.R., Crawley J.N. Mouse models of autism spectrum disorders: the challenge for behavioral genetics. American Journal of Medical Genetics 2006, 142C(1):40-51.
50. Moy S.S., Nadler J.J., Perez A., Barbaro R.P., Johns J.M., Magnuson T.R., Piven J., Crawley J.N. Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes, Brain and Behavior 2004, 3(5):287-302.
51. 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. Mouse behavioral tasks relevant to autism: phenotypes of 10 inbred strains. Behavioural Brain Research 2007, 176(1):4-20.
52. 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., Crawley J.N. Automated apparatus for quantitation of social approach behaviors in mice. Genes, Brain and Behavior 2004, 3(5):303-314.
53. National Science Foundation, n.d. A Timeline of NSF History. Retrieved from: http://www.nsf.gov/about/history/overview-50.jsp.
54. Nowak K., Meyza K., Nikolaev E., Hunt M.J., Kasicki S. Local blockade of NMDA receptors in the rat prefrontal cortex increases c-Fos expression in multiple subcortical regions. Acta Neurobiologiae Experimentalis (Warsaw) 2012, 72(3):207-218.
55. O'Leary O.F., Cryan J.F. Towards translational rodent models of depression. Cell and Tissue Research 2013, (Epub ahead of print).
56. Office of NIH History, n.d. Introduction: A Short History of the National Institutes of Health. Retrieved from: http://history.nih.gov/exhibits/history/index.html.
57. Olsen R.W., Sieghart W. GABA A receptors: subtypes provide diversity of function and pharmacology. Neuropharmacology 2009, 56(1):141-148.
58. Patterson P.H. Infectious Behavior: Brain-Immune Connections in Autism, Schizophrenia, and Depression 2011, MIT Press, Cambridge.
59. Pearson B.L., Corley M.J., Vasconcellos A., Blanchard D.C., Blanchard R.J. Heparan sulfate deficiency in autistic postmortem brain tissue from the subventricular zone of the lateral ventricles. Behavioural Brain Research 2013, 243:138-145.
60. Pearson B.L., Pobbe R.L., Defensor E.B., Oasay L., Bolivar V.J., Blanchard D.C., Blanchard R.J. Motor and cognitive stereotypies in the BTBR T+tf/J mouse model of autism. Genes, Brain and Behavior 2011, 10(2):228-235.
61. Pellis S.M., McKenna M. What do rats find rewarding in play fighting?-an analysis using drug-induced non-playful partners. Behavioural Brain Research 1995, 68(1):65-73.
62. Perkins A.M., Cooper A., Abdelall M., Smillie L.D., Corr P.J. Personality and defensive reactions: fear, trait anxiety, and threat magnification. Journal of Personality 2010, 78(3):1071-1090.
63. Perkins A.M., Corr P.J. Reactions to threat and personality: psychometric differentiation of intensity and direction dimensions of human defensive behaviour. Behavioural Brain Research 2006, 169(1):21-28.
64. Perkins A.M., Inchley-Mort S.L., Pickering A.D., Corr P.J., Burgess A.P. A facial expression for anxiety. Journal of Personality and Social Psychology 2012, 102(5):910-924.
65. Perkins A.M., Kemp S.E., Corr P.J. Fear and anxiety as separable emotions: an investigation of the revised reinforcement sensitivity theory of personality. Emotion 2007, 7(2):252-261.
66. Pobbe R.L., Defensor E.B., Pearson B.L., Bolivar V.J., Blanchard D.C., Blanchard R.J. General and social anxiety in the BTBR T+tf/J mouse strain. Behavioural Brain Research 2011, 216(1):446-451.
67. Pobbe R.L., Pearson B.L., Blanchard D.C., Blanchard R.J. Oxytocin receptor and Mecp2 308/Y knockout mice exhibit altered expression of autism-related social behaviors. Physiology and Behavior 2012, 107(5):641-648.
68. Richter S.H., Garner J.P., Würbel H. Environmental standardization: cure or cause of poor reproducibility in animal experiments?. Nature Methods 2009, 6(4):257-261.
69. Rodgers R.J., Johnson N.J. Factor analysis of spatiotemporal and ethological measures in the murine elevated plus-maze test of anxiety. Pharmacology Biochemistry and Behavior 1995, 52(2):297-303.
70. Sarter M., Bruno J. Animal models in biological psychiatry. Textbook of Biological Psychiatry 2002, Wiley, Chichester. H. D'Haenen, H. Den Boer, P. Willner (Eds.).
71. Scattoni M.L., Ricceri L., Crawley J.N. Unusual repertoire of vocalizations in adult BTBR T+tf/J mice during three types of social encounters. Genes, Brain and Behavior 2011, 10(1):44-56.
72. Senju A., Johnson M.H. Atypical eye contact in autism: models, mechanisms and development. Neuroscience and Biobehavioral Reviews 2009, 33(8):1204-1214.
73. Shuhama R., Del-Ben C.M., Loureiro S.R., Graeff F.G. Defensive responses to threat scenarios in Brazilians reproduce the pattern of Hawaiian Americans and non-human mammals. Brazilian Journal of Medical and Biological Research 2008, 41(4):324-332.
74. Simpson E.H., Waltz J.A., Kellendonk C., Balsam P.D. Schizophrenia in translation: dissecting motivation in schizophrenia and rodents. Schizophrenia Bulletin 2012, 38(6):1111-1117.
75. TedxTalks. (Producer), 2013. Mental Disorders as Brain Disorders: Thomas Insel at TEDxCaltech [Video Webcast]. Retrieved from: http://www.youtube.com/watch?v=u4m65sbqbhY.
76. Tinbergen N. On aims and methods of Ethology. Zeitschrift für Tierpsychologie 1963, 20(4):410-433.
77. van der Staay F.J., Arndt S.S., Nordquist R.E. Evaluation of animal models of neurobehavioral disorders. Behavioral and Brain Functions 2009, 5:11.
78. Willner P. The validity of animal models of depression. Psychopharmacology (Berlin). 1984, 83(1):1-16.
79. Willner P. Animal models as simulations of depression. Trends in Pharmacological Sciences 1991, 12(4):131-136.
80. Willner P., Mitchell P.J. The validity of animal models of predisposition to depression. Behavioural Pharmacology 2002, 13(3):169-188.
81. World Health Organization World Health Statistics 2010 2010, 177 pp. WHO Press, Retrieved from: http://www.who.int/whosis/whostat/EN_WHS10_Full.pdf.
82. World Health Organization National health Account database, 2013. Health Expenditure, Total (% of GDP). The World Bank: Retrieved from: http://apps.who.int/nha/database/DataExplorerRegime.aspx.
83. Wöhr M., Roullet F.I., Crawley J.N. Reduced scent marking and ultrasonic vocalizations in the BTBR T+tf/J mouse model of autism. Genes, Brain and Behavior 2011, 10(1):35-43.
84. Yan H.C., Cao X., Das M., Zhu X.H., Gao T.M. Behavioral animal models of depression. Neuroscience Bulletin 2010, 26(4):327-337.
85. Yoneda A., Lendorf M.E., Couchman J.R., Multhaupt H.A. Breast and ovarian cancers: a survey and possible roles for the cell surface heparan sulfate proteoglycans. Journal of Histochemistry and Cytochemistry 2012, 60(1):9-21.
86. Zor R., Szechtman H., Hermesh H., Fineberg N.A., Eilam D. Manifestation of incompleteness in obsessive-compulsive disorder (OCD) as reduced functionality and extended activity beyond task completion. PLoS ONE 2011, 6(9):e25217.