Anxiety is correlated with running in adolescent female mice undergoing activity-based anorexia

Behavioral Neuroscience

Volumn 129, Issue 2, 2015, Pages 170-182

  Wable, Gauri S ^a   Min, Jung Yun ^a   Chen, Yi Wen ^a   Aoki, Chiye ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

Activity based anorexia; Anorexia nervosa; Anxiety; Exercise; Food restriction

Indexed keywords

ADOLESCENT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOREXIA NERVOSA; ANXIETY; ARTICLE; BEHAVIOR CHANGE; BEHAVIOR CONTROL; CONTROLLED STUDY; DIET RESTRICTION; DISEASE ASSOCIATION; DISEASE SEVERITY; ELEVATED PLUS MAZE TEST; EXERCISE; EXPERIMENTAL MODEL; FEMALE; MOUSE; NONHUMAN; OPEN FIELD TEST; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; WEIGHT REDUCTION; ANIMAL; C57BL MOUSE; DISEASE MODEL; EATING; PATHOPHYSIOLOGY; PSYCHOLOGY; RUNNING;

ANIMALS; ANOREXIA NERVOSA; ANXIETY; DISEASE MODELS, ANIMAL; EATING; FEMALE; MICE; MICE, INBRED C57BL; RUNNING;

EID: 84925766685     PISSN: 07357044     EISSN: 19390084     Source Type: Journal    
DOI: 10.1037/bne0000040     Document Type: Article

References (73)

1. Almeida, S. S., Garcia, R. A., & de Oliveira, L. M. (1993). Effects of early protein malnutrition and repeated testing upon locomotor and exploratory behaviors in the elevated plus-maze. Physiology & Behavior, 54, 749-752. http://dx.doi.org/10.1016/0031-9384(93)90086-U
2. Aoki, C., Sabaliauskas, N., Chowdhury, T., Min, J. Y., Colacino, A. R., Laurino, K., & Barbarich-Marsteller, N. C. (2012). Adolescent female rats exhibiting activity-based anorexia express elevated levels of GABA(A) receptor _4 and _ subunits at the plasma membrane of hippocampal CA1 spines. Synapse, 66, 391-407. http://dx.doi.org/10.1002/syn.21528
3. Aoki, C., Wable, G., Chowdhury, T. G., Sabaliauskas, N. A., Laurino, K., & Barbarich-Marsteller, N. C. (2014). α4βδ-GABAARs in the hippocampal CA1 as a biomarker for resilience to activity-based anorexia. Neuroscience, 265, 108-123. http://dx.doi.org/10.1016/j.neuroscience .2014.01.011
4. American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington, VA: American Psychiatric Publishing.
5. Bannai, C., Kuzuya, N., Koide, Y., Fujita, T., Itakura, M., Kawai, K., & Yamashita, K. (1988). Assessment of the relationship between serum thyroid hormone levels and peripheral metabolism in patients with anorexia nervosa. Endocrinologia Japonica, 35, 455-462. http://dx.doi .org/10.1507/endocrj1954.35.455
6. Birmingham, C. L., Su, J., Hlynsky, J. A., Goldner, E. M., & Gao, M. (2005). The mortality rate from anorexia nervosa. International Journal of Eating Disorders, 38, 143-146. http://dx.doi.org/10.1002/eat.20164
7. Bond, N., & Giusto, E. D. (1977). Open-field behavior as a function of age, sex, and repeated trials. Psychological Reports, 41, 571-574. http://dx .doi.org/10.2466/pr0.1977.41.2.571
8. Breus, M. J., & O'Connor, P. J. (1998). Exercise-induced anxiolysis: A test of the "time out" hypothesis in high anxious females. Medicine & Science in Sports & Exercise, 30, 1107-1112. http://dx.doi.org/10.1097/00005768-199807000-00013
9. Bronstein, P. M. (1972). Repeated trials with the albino rat in the open field as a function of age and deprivation. Journal of Comparative and Physiological Psychology, 81, 84-93. http://dx.doi.org/10.1037/h0033361
10. Bronstein, P. M. (1973). Replication report: Age and open-field activity of rats. Psychological Reports, 32, 403-406. http://dx.doi.org/10.2466/pr0.1973.32.2.403
11. Bronstein, P. M., Wolkoff, F. D., & Levine, W. J. (1975). Sex-related differences in rats open-field activity. Behavioral Biology, 13, 133-138. http://dx.doi.org/10.1016/S0091-6773(75)90913-X
12. Bulik, C. M., Slof-Op't Landt, M. C., van Furth, E. F., & Sullivan, P. F. (2007). The genetics of anorexia nervosa. Annual Review of Nutrition, 27, 263-275. http://dx.doi.org/10.1146/annurev.nutr.27.061406.093713
13. Cador, M., Robbins, T. W., & Everitt, B. J. (1989). Involvement of the amygdala in stimulus-reward associations: Interaction with the ventral striatum. Neuroscience, 30, 77-86. http://dx.doi.org/10.1016/0306-4522(89)90354-0
14. Carola, V., D'Olimpio, F., Brunamonti, E., Mangia, F., & Renzi, P. (2002). Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behavioural Brain Research, 134, 49-57. http://dx.doi.org/10.1016/S0166-4328 (01)00452-1
15. Chowdhury, T. G., Wable, G. S., Sabaliauskas, N. A., & Aoki, C. (2013). Adolescent female C57BL/6 mice with vulnerability to activity-based anorexia exhibit weak inhibitory input onto hippocampal CA1 pyramidal cells. Neuroscience, 241, 250-267. http://dx.doi.org/10.1016/j .neuroscience.2013.03.020
16. Dallman, M. F., Akana, S. F., Bhatnagar, S., Bell, M. E., Choi, S., Chu, A., Viau, V. (1999). Starvation: Early signals, sensors, and sequelae. Endocrinology, 140, 4015-4023.
17. Davis, C., Katzman, D. K., & Kirsh, C. (1999). Compulsive physical activity in adolescents with anorexia nervosa: A psychobehavioral spiral of pathology. Journal of Nervous and Mental Disease, 187, 336-342. http://dx.doi.org/10.1097/00005053-199906000-00002
18. Duclos, M., Bouchet, M., Vettier, A., & Richard, D. (2005). Genetic differences in hypothalamic-pituitary-adrenal axis activity and food restriction-induced hyperactivity in three inbred strains of rats. Journal of Neuroendocrinology, 17, 740-752. http://dx.doi.org/10.1111/j.1365-2826.2005.01367.x
19. Duclos, M., Gatti, C., Bessière, B., & Mormède, P. (2009). Tonic and phasic effects of corticosterone on food restriction-induced hyperactivity in rats. Psychoneuroendocrinology, 34, 436-445. http://dx.doi.org/10.1016/j.psyneuen.2008.10.008
20. Epling, W. F., Pierce, D., & Stefan, L. (1983). A theory of activity-based anorexia. International Journal of Eating Disorders, 3, 27-46. http://dx .doi.org/10.1002/1098-108X(198323)3:1_27::AID-EAT22600301043.0.CO;2-T
21. Epling, W. F., & Pierce, W. D. (1996). Activity anorexia: Theory, research, and treatment. Mahwah: Erlbaum.
22. Escobar, C., Cailotto, C., Angeles-Castellanos, M., Delgado, R. S., & Buijs, R. M. (2009). Peripheral oscillators: The driving force for food-anticipatory activity. European Journal of Neuroscience, 30, 1665-1675. http://dx.doi.org/10.1111/j.1460-9568.2009.06972.x
23. Evans, J., Sun, Y., McGregor, A., & Connor, B. (2012). Allopregnanolone regulates neurogenesis and depressive/anxiety-like behaviour in a social isolation rodent model of chronic stress. Neuropharmacology, 63, 1315-1326. http://dx.doi.org/10.1016/j.neuropharm.2012.08.012
24. Fairburn, C. G., & Harrison, P. J. (2003). Eating disorders. The Lancet, 361, 407-416. http://dx.doi.org/10.1016/S0140-6736(03)12378-1
25. File, S. E. (1993). The interplay of learning and anxiety in the elevated plus-maze. Behavioural Brain Research, 58, 199-202. http://dx.doi.org/10.1016/0166-4328(93)90103-W
26. File, S. E., Mabbutt, P. S., & Hitchcott, P. K. (1990). Characterisation of the phenomenon of "one-trial tolerance" to the anxiolytic effect of chlordiazepoxide in the elevated plus-maze. Psychopharmacology, 102, 98-101. http://dx.doi.org/10.1007/BF02245751
27. Finger, B. C., Dinan, T. G., & Cryan, J. F. (2010). Leptin-deficient mice retain normal appetitive spatial learning yet exhibit marked increases in anxiety-related behaviours. Psychopharmacology, 210, 559-568. http://dx.doi.org/10.1007/s00213-010-1858-z
28. Fiore, F., Ruggiero, G. M., & Sassaroli, S. (2014). Emotional dysregulation and anxiety control in the psychopathological mechanism underlying drive for thinness. Frontiers in Psychiatry, 5, 43. http://dx.doi.org/10.3389/fpsyt.2014.00043
29. Gan, J. O., Bowline, E., Lourenco, F. S., & Pickel, V. M. (2014). Adolescent social isolation enhances the plasmalemmal density of NMDA NR1 subunits in dendritic spines of principal neurons in the basolateral amygdala of adult mice. Neuroscience, 258, 174-183. http://dx.doi.org/10.1016/j.neuroscience.2013.11.003
30. Gelegen, C., Collier, D. A., Campbell, I. C., Oppelaar, H., van den Heuvel, J., Adan, R. A., & Kas, M. J. (2007). Difference in susceptibility to activity-based anorexia in two inbred strains of mice. European Neuropsychopharmacology, 17, 199-205. http://dx.doi.org/10.1016/j .euroneuro.2006.04.007
31. Gelegen, C., van den Heuvel, J., Collier, D. A., Campbell, I. C., Oppelaar, H., Hessel, E., & Kas, M. J. (2008). Dopaminergic and brain-derived neurotrophic factor signalling in inbred mice exposed to a restricted feeding schedule. Genes, Brain & Behavior, 7, 552-559. http://dx.doi .org/10.1111/j.1601-183X.2008.00394.x
32. Golden, N. H., & Shenker, I. R. (1992). Amenorrhrea in anorexia nervosa:Etiology and implications. Adolescent Medicine (Philadelphia, PA), 3, 503-518.
33. Golden, N. H., & Shenker, I. R. (1994). Amenorrhea in anorexia nervosa. Neuroendocrine control of hypothalamic dysfunction. International Journal of Eating Disorders, 16, 53-60. http://dx.doi.org/10.1002/1098-108X(199407)16:1_53::AID-EAT22601601053.0.CO;2-V
34. Gutierrez, E. (2013). A rat in the labyrinth of anorexia nervosa: Contributions of the activity-based anorexia rodent model to the understanding of anorexia nervosa. International Journal of Eating Disorders, 46, 289-301. http://dx.doi.org/10.1002/eat.22095
35. Hall, J. F., & Hanford, P. V. (1954). Activity as a function of a restricted feeding schedule. Journal of Comparative and Physiological Psychology, 47, 362-363. http://dx.doi.org/10.1037/h0060276
36. Hebebrand, J., Exner, C., Hebebrand, K., Holtkamp, C., Casper, R. C., Remschmidt, H., Klingenspor, M. (2003). Hyperactivity in patients with anorexia nervosa and in semistarved rats: Evidence for a pivotal role of hypoleptinemia. Physiology & Behavior, 79, 25-37. http://dx.doi .org/10.1016/S0031-9384(03)00102-1
37. Hillard, C. J. (2014). Stress regulates endocannabinoid-CB1 receptor signaling. Advance online publication. Seminars in Immunology, 26, 380-388. http://dx.doi.org/10.1016/j.smim.2014.04.001
38. Holtkamp, K., Hebebrand, J., & Herpertz-Dahlmann, B. (2004). The contribution of anxiety and food restriction on physical activity levels in acute anorexia nervosa. International Journal of Eating Disorders, 36, 163-171. http://dx.doi.org/10.1002/eat.20035
39. Huttunen, P., & Myers, R. D. (1986). Tetrahydro-beta-carboline microinjected into the hippocampus induces an anxiety-like state in the rat. Pharmacology, Biochemistry and Behavior, 24, 1733-1738. http://dx .doi.org/10.1016/0091-3057(86)90513-7
40. Joëls, M., Sarabdjitsingh, R. A., & Karst, H. (2012). Unraveling the time domains of corticosteroid hormone influences on brain activity: Rapid, slow, and chronic modes. Pharmacological Reviews, 64, 901-938. http://dx.doi.org/10.1124/pr.112.005892
41. Kaye, W. H., Bulik, C. M., Thornton, L., Barbarich, N., & Masters, K. (2004). Comorbidity of anxiety disorders with anorexia and bulimia nervosa. The American Journal of Psychiatry, 161, 2215-2221. http://dx.doi.org/10.1176/appi.ajp.161.12.2215
42. Kierniesky, N., Sick, T., & Kruppenbacher, F. (1977). Open-field activity of albino rats as a function of sex, age, and repeated testing. Psychological Reports, 40, 1255-1260. http://dx.doi.org/10.2466/pr0.1977.40.3c.1255
43. Klenotich, S. J., & Dulawa, S. C. (2012). The activity-based anorexia mouse model. Methods in Molecular Biology (Clifton, NJ), 829, 377-393. http://dx.doi.org/10.1007/978-1-61779-458-2_25
44. Lee, C., & Rodgers, R. J. (1990). Antinociceptive effects of elevated plus-maze exposure: Influence of opiate receptor manipulations. Psychopharmacology, 102, 507-513. http://dx.doi.org/10.1007/BF02247133
45. Lister, R. G. (1987). The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology, 92, 180-185. http://dx.doi.org/10.1007/BF00177912
46. Liu, J., Perez, S. M., Zhang, W., Lodge, D. J., & Lu, X. Y. (2011). Selective deletion of the leptin receptor in dopamine neurons produces anxiogenic-like behavior and increases dopaminergic activity in amygdala. Molecular Psychiatry, 16, 1024-1038. http://dx.doi.org/10.1038/mp.2011.36
47. Mantzoros, C., Flier, J. S., Lesem, M. D., Brewerton, T. D., & Jimerson, D. C. (1997). Cerebrospinal fluid leptin in anorexia nervosa: Correlation with nutritional status and potential role in resistance to weight gain. The Journal of Clinical Endocrinology and Metabolism, 82, 1845-1851.
48. McDonald, A. J. (1998). Cortical pathways to the mammalian amygdala. Progress in Neurobiology, 55, 257-332. http://dx.doi.org/10.1016/S0301-0082(98)00003-3
49. Moscarello, J. M., Ben-Shahar, O., & Ettenberg, A. (2009). Effects of food deprivation on goal-directed behavior, spontaneous locomotion, and c-Fos immunoreactivity in the amygdala. Behavioural Brain Research, 197, 9-15. http://dx.doi.org/10.1016/j.bbr.2008.07.025
50. Myers, B., & Greenwood-Van Meerveld, B. (2007). Corticosteroid receptor-mediated mechanisms in the amygdala regulate anxiety and colonic sensitivity. American Journal of Physiology Gastrointestinal and Liver Physiology, 292, G1622-G1629. http://dx.doi.org/10.1152/ajpgi.00080.2007
51. Nakazato, M., Hashimoto, K., Shimizu, E., Niitsu, T., & Iyo, M. (2012). Possible involvement of brain-derived neurotrophic factor in eating disorders. IUBMB Life, 64, 355-361. http://dx.doi.org/10.1002/iub.1012
52. Patton, D. F., & Mistlberger, R. E. (2013). Circadian adaptations to meal timing: Neuroendocrine mechanisms. Frontiers in Neuroscience, 7, 1-14. http://dx.doi.org/10.3389/fnins.2013.00185
53. Peñas-Lledó, E., Vaz Leal, F. J., & Waller, G. (2002). Excessive exercise in anorexia nervosa and bulimia nervosa: Relation to eating characteristics and general psychopathology. International Journal of Eating Disorders, 31, 370-375. http://dx.doi.org/10.1002/eat.10042
54. Piazza, P. V., Rougé-Pont, F., Deroche, V., Maccari, S., Simon, H., & Le Moal, M. (1996). Glucocorticoids have state-dependent stimulant effects on the mesencephalic dopaminergic transmission. Proceedings of the National Academy of Sciences, United States of America, 93, 8716-8720. http://dx.doi.org/10.1073/pnas.93.16.8716
55. Pietropaolo, S., Sun, Y., Li, R., Brana, C., Feldon, J., & Yee, B. K. (2008). The impact of voluntary exercise on mental health in rodents: A neuro-plasticity perspective. Behavioral Brain Research, 192, 42-60. http://dx.doi.org/10.1016/j.bbr.2008.03.014
56. Ponder, C. A., Munoz, M., Gilliam, T. C., & Palmer, A. A. (2007). Genetic architecture of fear conditioning in chromosome substitution strains:Relationship to measures of innate (unlearned) anxiety-like behavior. Mammalian Genome, 18, 221-228. http://dx.doi.org/10.1007/s00335-007-9013-9
57. Rhodes, J. S., Garland, T., Jr., & Gammie, S. C. (2003). Patterns of brain activity associated with variation in voluntary wheel-running behavior. Behavioral Neuroscience, 117, 1243-1256. http://dx.doi.org/10.1037/0735-7044.117.6.1243
58. Riddle, M. C., McKenna, M. C., Yoon, Y. J., Pattwell, S. S., Santos, P. M., Casey, B. J., & Glatt, C. E. (2013). Caloric restriction enhances fear extinction learning in mice. Neuropsychopharmacology, 38, 930-937. http://dx.doi.org/10.1038/npp.2012.268
59. Rodgers, R. J., Lee, C., & Shepherd, J. K. (1992). Effects of diazepam on behavioural and antinociceptive responses to the elevated plus-maze in male mice depend upon treatment regimen and prior maze experience. Psychopharmacology, 106, 102-110. http://dx.doi.org/10.1007/BF02253596
60. Rodgers, R. J., & Shepherd, J. K. (1993). Influence of prior maze experience on behaviour and response to diazepam in the elevated plus-maze and light/dark tests of anxiety in mice. Psychopharmacology, 113, 237-242. http://dx.doi.org/10.1007/BF02245704
61. Routtenberg, A., & Kuznesof, A. W. (1967). Self-starvation of rats living in activity wheels on a restricted feeding schedule. Journal of Comparative and Physiological Psychology, 64, 414-421. http://dx.doi.org/10.1037/h0025205
62. Russell, P. A., & Williams, D. I. (1973). Effects of repeated testing on rats' locomotor activity in the open-field. Animal Behaviour, 21, 109-111. http://dx.doi.org/10.1016/S0003-3472(73)80047-8
63. Sciolino, N. R., & Holmes, P. V. (2012). Exercise offers anxiolytic potential:A role for stress and brain noradrenergic-galaninergic mechanisms. Neuroscience and Biobehavioral Reviews, 36, 1965-1984. http://dx.doi .org/10.1016/j.neubiorev.2012.06.005
64. Shroff, H., Reba, L., Thornton, L. M., Tozzi, F., Klump, K. L., Berrettini, W. H., Bulik, C. M. (2006). Features associated with excessive exercise in women with eating disorders. International Journal of Eating Disorders, 39, 454-461. http://dx.doi.org/10.1002/eat.20247
65. Singer, J. B., Hill, A. E., Nadeau, J. H., & Lander, E. S. (2005). Mapping quantitative trait loci for anxiety in chromosome substitution strains of mice. Genetics, 169, 855-862. http://dx.doi.org/10.1534/genetics.104.031492
66. Sullivan, P. F. (1995). Mortality in anorexia nervosa. The American Journal of Psychiatry, 152, 1073-1074. http://dx.doi.org/10.1176/ajp.152.7.1073
67. Treit, D., Menard, J., & Royan, C. (1993). Anxiogenic stimuli in the elevated plus-maze. Pharmacology, Biochemistry and Behavior, 44, 463-469. http://dx.doi.org/10.1016/0091-3057(93)90492-C
68. Tye, K. M., Prakash, R., Kim, S. Y., Fenno, L. E., Grosenick, L., Zarabi, H., Deisseroth, K. (2011). Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature, 471, 358-362. http://dx.doi .org/10.1038/nature09820
69. Valle, F. P. (1971). Rats' performance on repeated tests in the open field as a function of age. Psychonomic Science, 23, 333-334. http://dx.doi .org/10.3758/BF03336137
70. van Gaalen, M. M., & Steckler, T. (2000). Behavioural analysis of four mouse strains in an anxiety test battery. Behavioural Brain Research, 115, 95-106. http://dx.doi.org/10.1016/S0166-4328(00)00240-0
71. Wable, G. S., Barbarich-Marsteller, N. C., Chowdhury, T. G., Sabaliauskas, N. A., Farb, C. R., & Aoki, C. (2014). Excitatory synapses on dendritic shafts of the caudal basal amygdala exhibit elevated levels of GABAA receptor _4 subunits following the induction of activity-based anorexia. Synapse (New York, NY), 68, 1-15. http://dx.doi.org/10.1002/syn.21690
72. Walf, A. A., & Frye, C. A. (2007). The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nature Protocols, 2, 322-328. http://dx.doi.org/10.1038/nprot.2007.44
73. Yamamoto, Y., Tanahashi, T., Kawai, T., Chikahisa, S., Sakurako, K., Kensei, N., Rokutan, K. (2009). Changes in behavior and gene expression induced by caloric restriction in C57BL/6 mice. Physiological Genomics, 39, 227-235.