Behavioral and physiological consequences of enrichment loss in rats

Psychoneuroendocrinology

Volumn 77, Issue , 2017, Pages 37-46

  Smith, Brittany L ^a   Lyons, Carey E ^a   Correa, Fernanda Guilhaume ^a   Benoit, Stephen C ^a   Myers, Brent ^a   Solomon, Matia B ^a   Herman, James P ^a  

^a UNIVERSITY OF CINCINNATI   (United States)

Author keywords

Depression; Environmental enrichment; Imipramine; Loss; Stress; Weight gain

Indexed keywords

CORTICOTROPIN; IMIPRAMINE; ANTIDEPRESSANT AGENT;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AVERSIVE BEHAVIOR; BEHAVIOR CHANGE; CHRONIC STRESS; CONTROLLED STUDY; CORTICOTROPIN BLOOD LEVEL; DEPRESSION; ENVIRONMENTAL ENRICHMENT; EXERCISE; FEEDING BEHAVIOR; FORCED SWIM TEST; HELPLESSNESS; HYPOTHALAMUS HYPOPHYSIS SYSTEM; LIPID DIET; MALE; NONHUMAN; OPEN FIELD TEST; OVERNUTRITION; PHYSICAL STIMULATION; PRIORITY JOURNAL; PSYCHOPHYSIOLOGY; RAT; REWARD; RUNNING; SOCIAL BEHAVIOR; SOCIAL INTERACTION TEST; SUCROSE PREFERENCE TEST; ANIMAL; ANIMAL HOUSING; DIET; DISEASE MODEL; DRUG EFFECTS; ENVIRONMENT; HYPOPHYSIS ADRENAL SYSTEM; MENTAL STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; ANTIDEPRESSIVE AGENTS; BEHAVIOR, ANIMAL; DEPRESSION; DIET; DISEASE MODELS, ANIMAL; ENVIRONMENT; FEEDING BEHAVIOR; HOUSING, ANIMAL; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; PITUITARY-ADRENAL SYSTEM; RATS; REWARD; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL;

EID: 85006944690     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2016.11.040     Document Type: Article

References (53)

1. Bakos, J., Hlavacova, N., Rajman, M., Ondicova, K., Koros, C., Kitraki, E., Steinbusch, H.W., Jezova, D., Enriched environment influences hormonal status and hippocampal brain derived neurotrophic factor in a sex dependent manner. Neuroscience 164:December (2) (2009), 788–797.
2. Belke, T.W., Studies of wheel-running reinforcement: parameters of Herrnstein's (1970) response-strength equation vary with schedule order. J. Exp. Anal. Behav. 73 (2000), 319–331.
3. Belz, E.E., Kennell, J.S., Czambel, R.K., Rubin, R.T., Rhodes, M.E., Environmental enrichment lowers stress-responsive hormones in singly housed male and female rats. Pharmacol. Biochem. Behav. 76:December (3–4) (2003), 481–486.
4. Bevins, R.A., Bardo, M.T., Conditioned increase in place preference by access to novel objects: antagonism by MK-801. Behav. Brain Res. 99 (1999), 53–60.
5. Brenes Sáenz, J.C., Villagra, O.R., Fornaguera Trías, J., Factor analysis of Forced Swimming test, Sucrose Preference test and Open Field test on enriched, social and isolated reared rats. Behav. Brain Res. 169:April (1) (2006), 57–65.
6. Brenes, J.C., Fornaguera, J., Effects of environmental enrichment and social isolation on sucrose consumption and preference: associations with depressive-like behavior and ventral striatum dopamine. Neurosci. Lett. 436:May (2) (2008), 278–282.
7. Brenes, J.C., Rodríguez, O., Fornaguera, J., Differential effect of environment enrichment and social isolation on depressive-like behavior, spontaneous activity and serotonin and norepinephrine concentration in prefrontal cortex and ventral striatum. Pharmacol. Biochem. Behav. 89:March (1) (2008), 85–93.
8. Choi, D.L., Davis, J.F., Fitzgerald, M.E., Benoit, S.C., The role of orexin-A in food motivation, reward-based feeding behavior and food-induced neuronal activation in rats. Neuroscience 167:April (1) (2010), 11–20.
9. Chou, K.L., Yu, K.M., Atypical depressive symptoms and obesity in a national sample of older adults with major depressive disorder. Depress. Anxiety 30:June (6) (2013), 574–579.
10. Christie-Seely, J., Life stress and illness: a systems approach. Can. Fam. Phys. 29:March (1983), 533–540.
11. Crofton, E.J., Zhang, Y., Green, T.A., Inoculation stress hypothesis of environmental enrichment. Neurosci. Biobehav. Rev. 49:February (2015), 19–31.
12. Cryan, J.F., Page, M.E., Lucki, I., Differential behavioral effects of the antidepressants reboxetine: fluoxetine, and moclobemide in a modified forced swim test following chronic treatment. Psychopharmacology 182:November (3) (2005), 335–344.
13. Cryan, J.F., Valentino, R.J., Lucki, I., Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci. Biobehav. Rev. 29:4–5 (2005), 547–569.
14. Davis, J.F., Perello, M., Choi, D.L., Magrisso, I.J., Kirchner, H., Pfluger, P.T., Tschoep, M., Zigman, J.M., Benoit, S.C., GOAT induced ghrelin acylation regulates hedonic feeding. Horm. Behav. 62:November (5) (2012), 598–604.
15. Fava, M., Diagnosis and definition of treatment-resistant depression. Biol. Psychiatry 53:April (8) (2003), 649–659.
16. Flak, J.N., Solomon, M.B., Jankord, R., Krause, E.G., Herman, J.P., Identification of chronic stress-activated regions reveals a potential recruited circuit in rat brain. Eur. J. Neurosci. 36:August (4) (2012), 2547–2555.
17. Francis, D.D., Diorio, J., Plotsky, P.M., Meaney, M.J., Environmental enrichment reverses the effects of maternal separation on stress reactivity. J. Neurosci. 22:September (18) (2002), 7840–7843.
18. Ganzini, L., McFarland, B.H., Cutler, D., Prevalence of mental disorders after catastrophic financial loss. J. Nerv. Ment. Dis. 178:November (11) (1990), 680–685.
19. Gold, P.W., Chrousos, G.P., Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs low CRH/NE states. Mol. Psychiatry 7:3 (2002), 254–275.
20. Green, T.A., Alibhai, I.N., Roybal, C.N., Winstanley, C.A., Theobald, D.E., Birnbaum, S.G., Graham, A.R., Unterberg, S., Graham, D.L., Vialou, V., Bass, C.E., Terwilliger, E.F., Bardo, M.T., Nestler, E.J., Environmental enrichment produces a behavioral phenotype mediated by low cyclic adenosine monophosphate response element binding (CREB) activity in the nucleus accumbens. Biol. Psychiatry 67:January (1) (2010), 28–35.
21. Greenwood, B.N., Foley, T.E., Le, T.V., Strong, P.V., Loughridge, A.B., Day, H.E., Fleshner, M., Long-term voluntary wheel running is rewarding and produces plasticity in the mesolimbic reward pathway. Behav. Brain Res. 217 (2011), 354–362.
22. Hong, S., Flashner, B., Chiu, M., ver Hoeve, E., Luz, S., Bhatnagar, S., Social isolation in adolescence alters behaviors in the forced swim and sucrose preference tests in female but not in male rats. Physiol. Behav. 105:January (2) (2012), 269–275.
23. Howell, D., Fundamental Statistics for the Behavioral Sciences. 8th edition, 2013, 424–428 Chapter 16.
24. Johnson, E.M., Traver, K.L., Hoffman, S.W., Harrison, C.R., Herman, J.P., Environmental enrichment protects against functional deficits caused by traumatic brain injury. Front. Behav. Neurosci., 21(May (7)), 2013, 44.
25. Konkle, A.T., Kentner, A.C., Baker, S.L., Stewart, A., Bielajew, C., Environmental-enrichment-related variations in behavioral, biochemical, and physiologic responses of Sprague-Dawley and Long Evans rats. J. Am. Assoc. Lab. Anim. Sci. 49:July (4) (2010), 427–436.
26. Kopp, B.L., Wick, D., Herman, J.P., Differential effects of homotypic vs: heterotypic chronic stress regimens on microglial activation in the prefrontal cortex. Physiol. Behav. 122:October (2013), 246–252.
27. Kovner, I., Taicher, G.Z., Mitchell, A.D., Calibration and validation of EchoMRI™ whole body composition analysis based on chemical analysis of piglets, in comparison with the same for DXA. Int. J. Body Compos. Res. 8:1 (2010), 17–29.
28. Krishnan, V., Nestler, E.J., Animal models of depression: molecular perspectives. Curr. Top. Behav. Neurosci. 7 (2011), 121–147.
29. Wang, L., Seelig, A., Wadsworth, S.M., McMaster, H., Alcaraz, J.E., Crum-Cianflone, N.F., Associations of military divorce with mental, behavioral, and physical health outcomes. BMC Psychiatry, 19(June (15)), 2015, 128.
30. Louilot, A., Le Moal, M., Simon, H., Differential reactivity of dopaminergic neurons in the nucleus accumbens in response to different behavioral situations An in vivo voltammetric study in free moving rats. Brain Res. 397 (1986), 395–400.
31. McKlveen, J.M., Myers, B., Flak, J.N., Bundzikova, J., Solomon, M.B., Seroogy, K.B., Herman, J.P., Role of prefrontal cortex glucocorticoid receptors in stress and emotion. Biol. Psychiatry 74:November (9) (2013), 672–679.
32. Moncek, F., Duncko, R., Johansson, B.B., Jezova, D., Effect of environmental enrichment on stress related systems in rats. J. Neuroendocrinol. 16 (2004), 423–431.
33. Myers, B., Carvalho-Netto, E., Wick-Carlson, D., Wu, C., Naser, S., Solomon, M.B., Ulrich-Lai, Y.M., Herman, J.P., GABAergic signaling within a limbic-hypothalamic circuit integrates social and anxiety-like behavior with stress reactivity. Neuropsychopharmacology 41:May (6) (2016), 1530–1539.
34. Overstreet, D.H., Keeney, A., Hogg, S., Antidepressant effects of citalopram and CRF receptor antagonist CP-154,526 in a rat model of depression. Eur. J. Pharmacol. 492:May (2–3) (2004), 195–201.
35. Overstreet, D.H., Behavioral characteristics of rat lines selected for differential hypothermic responses to cholinergic or serotonergic agonists. Behav. Genet. 32:September (5) (2002), 335–348.
36. Packard, A.E., Ghosal, S., Herman, J.P., Woods, S.C., Ulrich-Lai, Y.M., Chronic variable stress improves glucose tolerance in rats with sucrose-induced prediabetes. Psychoneuroendocrinology 47:September (2014), 178–188.
37. Peña, Y., Prunell, M., Rotllant, D., Armario, A., Escorihuela, R.M., Enduring effects of environmental enrichment from weaning to adulthood on pituitary-adrenal function, pre-pulse inhibition and learning in male and female rats. Psychoneuroendocrinology 34:October (9) (2009), 1390–1404.
38. Puhl, M.D., Blum, J.S., Acosta-Torres, S., Grigson, P.S., Environmental enrichment protects against the acquisition of cocaine self-administration in adult male rats, but does not eliminate avoidance of a drug-associated saccharin cue. Behav. Pharmacol. 23:February (1) (2012), 43–53.
39. Rahe, R.H., Life-change measurement as a predictor of illness. Proc. R. Soc. Med. 61:November (11) Pt 1 (1968), 1124–1126.
40. Rebec, G.V., Grabner, C.P., Johnson, M., Pierce, R.C., Bardo, M.T., Transient increases in catecholaminergic activity in medial prefrontal cortex and nucleus accumbens shell during novelty. Neuroscience 76 (1997), 707–714.
41. Sikorski, C., Luppa, M., Heser, K., Ernst, A., Lange, C., Werle, J., Bickel, H., Mösch, E., Wiese, B., Prokein, J., Fuchs, A., Pentzek, M., König, H.H., Brettschneider, C., Scherer, M., Maier, W., Weyerer, S., Riedel-Heller, S.G., AgeCoDe Study Group, The role of spousal loss in the development of depressive symptoms in the elderly - implications for diagnostic systems. J. Affect. Disord. 161 (2014), 97–103.
42. Skwara, A.J., Karwoski, T.E., Czambel, R.K., Rubin, R.T., Rhodes, M.E., Influence of environmental enrichment on hypothalamic-pituitary-adrenal (HPA) responses to single-dose nicotine, continuous nicotine by osmotic mini-pumps, and nicotine withdrawal by mecamylamine in male and female rats. Behav. Brain Res. 234:September (1) (2012), 1–10.
43. Smith, B.L., Schmeltzer, S.N., Packard, B.A., Sah, R., Herman, J.P., Divergent effects of repeated restraint versus chronic variable stress on prefrontal cortical immune status after LPS injection. Brain Behav. Immun. 57:October (2016), 263–270.
44. Solinas, M., Chauvet, C., Thiriet, N., El Rawas, R., Jaber, M., Reversal of cocaine addiction by environmental enrichment. Proc. Natl. Acad. Sci. U. S. A. 105:November (44) (2008), 17145–17150.
45. Solomon, M.B., Wulsin, A.C., Rice, T., Wick, D., Myers, B., McKlveen, J., Flak, J.N., Ulrich-Lai, Y., Herman, J.P., The selective glucocorticoid receptor antagonist CORT 108297 decreases neuroendocrine stress responses and immobility in the forced swim test. Horm. Behav. 65:April (4) (2014), 363–371.
46. Stairs, D.J., Prendergast, M.A., Bardo, M.T., Environmental-induced differences in corticosterone and glucocorticoid receptor blockade of amphetamine self-administration in rats. Psychopharmacology (Berl). 218:November (1) (2011), 293–301.
47. Stuart, S.A., Butler, P., Munafò, M.R., Nutt, D.J., Robinson, E.S., A translational rodent assay of affective biases in depression and antidepressant therapy. Neuropsychopharmacology 38:August (9) (2013), 1625–1635.
48. Tsigos, C., Chrousos, G.P., Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J. Psychosom. Res. 53:October (4) (2002), 865–871.
49. Wiseman, T.A., Curtis, K., Lam, M., Foster, K., Incidence of depression, anxiety and stress following traumatic injury: a longitudinal study. Scand. J. Trauma Resusc. Emerg. Med., 28(March (23)), 2015, 29.
50. Wulsin, A.C., Herman, J.P., Solomon, M.B., Mifepristone decreases depression-like behavior and modulates neuroendocrine and central hypothalamic-pituitary-adrenocortical axis responsiveness to stress. Psychoneuroendocrinology 35:August (7) (2010), 1100–1112.
51. Wang, Y., Sareen, J., Afifi, T.O., Bolton, S.L., Johnson, E.A., Bolton, J.M., A population-based longitudinal study of recent stressful life events as risk factors for suicidal behavior in major depressive disorder. Arch. Suicide Res. 19:2 (2015), 202–217.
52. Yates, J.R., Beckmann, J.S., Meyer, A.C., Bardo, M.T., Concurrent choice for social interaction and amphetamine using conditioned place preference in rats: effects of age and housing condition. Drug Alcohol Depend. 129:May (3) (2013), 240–246.
53. van der Harsta, J.E., Fermonta, P.C.J., Bilstraa, A.E., Spruijta, B.M., Access to enriched housing is rewarding to rats as reflected by their anticipatory behavior. Anim. Behav. 66:September (3) (2003), 493–504.