Physical activity and environmental enrichment: Behavioural effects of exposure to different housing conditions in mice

• Autorzy: Rabadan R. , Ramos-Campos M. , Redolat R. , Mesa-Gresa P.
• Języki publikacji: EN

Abstrakty

EN

Enriched environments and exercise provide complex environmental stimulation that can induce emotional and cognitive changes; however, few studies have evaluated the effects of these two components on other behaviours, such as novelty seeking or pain sensitivity. The aim of the present study was to investigate the influence of voluntary physical activity provided through different housing conditions on anxiety, locomotor activity, pain sensitivity, and exploration. Male mice at postnatal day (PND) 21 and were randomly assigned to one of four different conditions on PND 28: Marlau cages (MC), a  standardized cage designed to provide a complex environment; physical exercise in large groups (PE‑8); physical exercise in small groups (PE‑4); or a standard environment (SE). After seven weeks, animals were evaluated in the hole‑board task, the elevated zero maze, actimeter, and hot plate test. In the hole‑board task, MC animals displayed more exploration than animals in the PE‑8 and PE‑4 groups, but no significant differences were observed between groups in the actimeter. In the elevated zero maze, MC and PE‑8 animals exhibited an anxiogenic‑like profile as compared to the SE group. When pain sensitivity was evaluated, the PE‑8 group displayed a higher sensitivity to noxious thermal stimuli than the SE group. These data suggest that the complexity of the environment in which physical activity and environmental stimulation are provided can influence animal behaviours such as novelty seeking, emotional response, and pain sensitivity. These animal models could be useful for designing more personalized interventions that include physical, social, and cognitive stimulation to promote a more active lifestyle in humans. Such interventions could be useful in the prevention and treatment of aging‑related decline or neurodegenerative diseases.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2019
• Tom: 79
• Numer: 4
• Opis fizyczny: p.374-385, fig.,ref.

Twórcy

autor

Rabadan R.

• Department of Psychobiology, Faculty of Psychology, University of Valencia, Valencia, Spain

autor

Ramos-Campos M.

• Department of Psychobiology, Faculty of Psychology, University of Valencia, Valencia, Spain

autor

Redolat R.

• Department of Psychobiology, Faculty of Psychology, University of Valencia, Valencia, Spain

autor

Mesa-Gresa P.

• Department of Psychobiology, Faculty of Psychology, University of Valencia, Valencia, Spain

Bibliografia

• Almeida, C, DeMaman, A, Kusuda, R, Cadetti F, Ravanelli MI, Queiroz AL, Sousa TA, Zanon S, Silveira LR, Lucas G (2015) Exercise therapy normal‑ izes BDNF upregulation and glial hyperactivity in mouse model of neu‑ ropathic pain. Pain 156: 504–513.
• Aujnarain AB, Luo OD, Taylor N, Lai JKY, Foster JA (2018) Effects of exercise and enrichment on behaviour in CD‑1 mice. Behav Brain Res 342: 43–50.
• Azar, TA, Sharp, JL, Lawson, DM (2012) Effects of cage enrichment on heart rate, blood pressure, and activity of female Sprague‑Dawley and sponta‑ neously hypertensive rats at rest and after acute challenges.  J Am Assoc Lab Anim Sci 51: 339–344.
• Basso JC, Morrell JI (2017) Using wheel availability to shape running be‑ havior of the rat towards improved behavioral and neurobiological out‑ comes. J Neurosci Methods 290: 13–23.
• Boissier JM, Simon P, Lwoff JM (1964) Use of a particular mouse reaction (hole board method) for the study of psychotropic drugs. Therapie 19: 571–583.
• Buchhold B,  Mogoanta  L,  Suofu Y, Hamm A, Walker  L, Kessler C, Popa‑Wagner A (2007)  Environmental enrichment improves function‑ al and neuropathological indices following stroke in young and aged rats. Restor Neurol Neurosci 25: 467–484. 
• Chapillon P, Manneché C, Belzung C, Caston, J (1999) Rearing environmen‑ tal enrichment in two inbred strains of mice: Effects on emotional reac‑ tivity. Behav Genet 29: 41–46.
• Clemenson GD, Deng W, Gage, FH (2015) Environmental enrichment and neurogenesis: From mice to humans. Curr Opin Behav Sci 4: 56–62. 
• Daffner KR (2010) Promoting successful cognitive aging: A comprehensive review. J Alzheimers Dis 19: 1101–1122.
• De Bartolo P, Leggio MG, Mandolesi L, Foti F, Gelfo F, Ferlazzo F, Petrosini L (2008)  Environmental enrichment mitigates the effects of basal fore‑ brain lesions on cognitive flexibility. Neuroscience 154: 444–453. 
• Dhanushkodi A, Bindu B, Raju TR, Kutty BM (2007) Exposure to enriched environment improves spatial learning performances and enhances cell density but not choline acetyltransferase activity in the hippocampus of ventral subicular‑lesioned rats. Behav Neurosci 121: 491–500. 
• Du Z, Li Y, Li J, Zhou C, Li F, Yang X (2018) Physical activity can improve cognition in patients with Alzheimer’s disease: a systematic review and meta‑analysis of randomized controlled trials. Clin Interv Aging 13: 1593–1603.
• Diniz DG, Foro CAR, Rego CMD, Gloria DA, De Oliveira FRR,  Paes JMP, Diniz CWP (2010) Environmental impoverishment and aging alter ob‑ ject recognition, spatial learning, and dentate gyrus astrocytes.  Eur J Neurosci 32: 509–519. 
• Fabel K, Wolf SA,  Ehninger D,  Babu H, Leal‑Galicia P, Kempermann G (2009) Additive effects of physical exercise and environmental enrich‑ ment on adult hippocampal neurogenesis in mice. Front Neurosci  3: 1–7.
• Falls WA, Fox JH, MacAulay CM (2010) Voluntary exercise improves both learning and consolidation of cued conditioned fear in C57 mice. Behav Brain Res 207: 321–331.
• Fares RP, Belmeguenai A, Sanchez PE, Kouchi HY, Bodennec J, Morales A, Bezin  L (2013) Standardized environmental enrichment supports en‑ hanced brain plasticity in healthy rats and prevents cognitive impair‑ ment in epileptic rats.  PLoS ONE 8: e53888.
• Fares RP, Fares RP, Kouchi H, Bezin L (2012) Standardized environmental enrichment for rodents in Marlau cage. Protocol Exchange 1–12.  Fischer A (2016) Environmental enrichment as a method to improve cogni‑ tive function.What can we learn from animal models? Neuroimage 131: 42–47.
• Fuss J, Ben Abdallah NM, Vogt MA, Touma C, Pacifici PG, Palme R, Witzemann V, Hellweg R, Gass P (2010) Voluntary exercise induces anx‑ iety‑like behavior in adult C57BL/6J mice correlating with hippocampal neurogenesis. Hippocampus 20: 364–376.
• Gabriel, AF,  Paoletti, G, Seta D Della,  Panelli R, Marcus MAE,  Farabolli‑ ni F, Joosten, EAJ (2010) Enriched environment and the recovery from inflammatory pain: Social versus physical aspects and their interac‑ tion. Behav Brain Res 208: 90–95.
• Gelfo F, Mandolesi L, Serra L, Sorrentino G, Caltagirone C (2017) The neu‑ roprotective effects of experience on cognitive functions: Evidence from animal studies on the neurobiological bases of brain reserve. Neurosci‑ ence pii: S0306–4522(17)30551–1.
• Hughes RN, Collins MA (2010) Enhanced habituation and decreased anx‑ iety by environmental enrichment and possible attenuation of these effects by chronic α‑tocopherol (vitamin E) in aging male and female rats. Pharmacol Biochem Behav 94: 534–542.
• Kentrop J, Smid CR, Achterberg EJM, van IJzendoorn MH, Baker‑ mans‑Kranenbur MJ, Joëls M, van der Veen R (2018) Effects of maternal deprivation and complex housing on rat social behavior in adoles‑ cence and adulthood. Front Behav Neurosci 12: 193.
• Kimura LF, Mattaraia VGM, Picolo G (2019) Distinct environmental enrich‑ ment protocols reduce anxiety but differentially modulate pain sensitiv‑ ity in rats. Behav Brain Res 364: 442–446.
• Kobilo T, Liu QR, Gandhi K, Mughal M, Shaham, van Praag H (2011) Run‑ ning is the neurogenic and neurotrophic stimulus in environmental enrichment. Learn Mem 18: 605–609. 
• Leggio MG, Mandolesi L, Federico F, Spirito F, Ricci B, Gelfo F, Petrosini L (2005)  Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav Brain Res 163: 78–90. 
• Leon  M, Woo C (2018) Environmental enrichment and successful aging. Front Behav Neurosci 12: 155.
• Lima LV, DeSantana JM, Rasmussen LA, Sluka KA (2017) Short‑duration physicalactivity prevents the development of activity‑induced hyperalge‑ sia through opioidand serotoninergic mechanisms. Pain 158: 1697–1710.
• Livingston‑Thomas J, Nelson P,  Karthikeyan S,  Antonescu S, Jeffers  MS, Marzolini S, Corbett D (2016) Exercise and environmental enrichment as enablers of task‑specific neuroplasticity and stroke recovery.  Neu‑ rotherapeutics 13: 395–402.
• Mármol F, Sánchez J, Torres, MN, Chamizo VD (2017) Environmental enrich‑ ment in the absence of wheel running produces beneficial behavioural and anti‑oxidative effects in rats. Behav Processes 144: 66–71.
• Mason G, Würbel H (2016) What can be learnt from wheel‑running by wild mice, and how can we identify when wheel‑running is pathologi‑ cal? Proc R Soc B 283: 20150738.
• Mesa‑Gresa P, Pérez‑Martinez A, Redolat R (2013a) Environmental enrich‑ ment improves novel object recognition and enhances agonistic behav‑ ior in male mice. Aggress Behav 39: 269–279.
• Mesa‑Gresa P, Pérez‑Martinez A, Redolat R (2013b) Behavioral effects of combined environmental enrichment and chronic nicotine administra‑ tion in male NMRI mice. Physiol Behav 114–115: 65–76.
• Mesa‑Gresa P, Ramos‑Campos M, Redolat R (2014) Behavioral effects of different enriched environments in mice treated with the cholinergic agonist PNU 282987. Behav Proc 103: 117–124.
• Mesa‑Gresa P, Ramos‑Campos M, Redolat R (2016) Corticosterone levels and behavioral changes induced by simultaneous exposure to chron‑ ic social stress and enriched environments in NMRI male mice. Physiol Behav 158: 6–17. 
• Mesa‑Gresa P, Redolat R (2018) Nicotine and agonists of alpha 7 nicotinic ace‑ tylcholine receptors combined with environmental enrichment. In: Acetyl‑ choline Receptors in Health and Disease. Nova Science Publishers, In press. Moraska A, Fleshner  M (2001)  Voluntary physical activity prevents stress‑induced behavioral depression and anti‑KLH antibody suppres‑ sion. Am J Physiol Regul Integr Comp Physiol 281: R484–R489. 
• Mustroph ML, Chen S, Desai SC, Cay EB, DeYoung EK, Rhodes JS (2012) Aerobic exercise is the critical variable in an enriched environment that increases hippocampal neurogenesis and water maze learning in male C57BL/6J mice. Neuroscience 219: 62–71.
• Nithianantharajah J, Hannan AJ (2006)  Enriched environments, experi‑ ence‑dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7: 697–709.
• Nithianantharajah J, Hannan AJ (2009) The neurobiology of brain and cog‑ nitive reserve: Mental and physical activity as modulators of brain disor‑ ders. Prog Neurobiol 89: 369–382.
• Pang TY, Hannan AJ (2013) Enhancement of cognitive function in models of brain disease through environmental enrichment and physical activi‑ ty. Neuropharmacology 64: 515–528.
• Parent‑Vachon  M, Vachon P (2018) Environmental enrichment alleviates chronic pain in rats following a spared nerve injury to induce neuropath‑ ic pain. A preliminary study. Vet Med 10: 69–72.
• Pietropaolo S, Sun , Li R, Brana C, Feldon J, Yee BK (2008) The impact of voluntary exercise on mental health in rodents: A neuroplasticity per‑ spective. Behav Brain Res 192: 42–60.  
• Redolat R, Mesa‑Gresa P (2012) Potential benefits and limitations of en‑ riched environments and cognitive activity on age‑related behavioural decline. Curr Top Behav Neurosci 10: 293–316.
• Rogers J, Renoir T, Hannan AJ (2019) Gene‑environment interactions in‑ forming therapeutic approaches to cognitive and affective disorders. Neuropharmacology 145: 37–48. Sale A, Berardi N, Maffei L (2014) Environment and brain plasticity: towards an endogenous pharmacotherapy. Physiol Rev 94: 189–234.
• Sampedro‑Piquero P, Zancada‑Menendez C, Begega A, Rubio S, Arias JL (2013) Effects of environmental enrichment on anxiety responses, spa‑ tial memory and cytochrome c oxidase activity in adult rats. Brain Res Bull 98: 1–9.
• Sampedro‑Piquero P, Begega A (2017) Environmental enrichment as a pos‑ itive behavioral intervention across the lifespan. Curr Neuropharmacol 15: 459–470.
• Sampedro‑Piquero P, Álvarez‑Suárez P, Moreno‑Fernández RD, García‑Castro G, Cuesta M, Begega A (2018) Environmental enrichment results in both brain connectivity efficiency and selective improvement in dif‑ ferent behavioral tasks. Neuroscience 388: 374–383.
• Schoenfeld, TJ, Rada P, Pieruzzini PR, HsuehB, Gould E (2013) Physical exer‑ cise prevents stress‑induced activation of granule neurons and enhanc‑ es local inhibitor. J Neurosci 33: 7770–7777. 
• Shepherd JK, Grewal SS, Fletcher A, Bill DJ, Dourish CT (1994) Behavioural and pharmacological characterisation of the elevated “zero‑maze” as an animal model of anxiety. Psychopharmacology 116: 56–64.
• Shevtsova O, Tan YF, Merkley CM, Winocur G, Wojtowicz JM (2017) Ear‑ ly‑age running enhances activity of adult‑born dentate granule neurons following learning in rats. eNeuro 4: pii: ENEURO.0237–17.2017.
• Simpson J, Kelly JP (2011) The impact of environmental enrichment in lab‑ oratory rats‑Behavioural and neurochemical aspects. Behav Brain Res 222: 246–264.
• Smits JAJ, Berry AC,  Rosenfield D, Powers MB, Behar E, Otto MW (2008) Reducing anxiety sensitivity with exercise. Depress Anxiety 25: 689–699. 
• Sztainberg Y, Chen A (2010)  An environmental enrichment model for mice. Nat Protoc 5: 1535–1539.
• Vachon P, Millecamps  M, Low  L, Thompsosn SJ, Pailleux F, Beaudry F, Bushnell CM, Stone LS (2013) Alleviation of chronic neuropathic pain by environmental enrichment in mice well after the establishment of chronic pain. Behav Brain Funct 9: 22.
• Van der Veen R., Kentrop J, van der Tas  L, Loi  M, van IJzendoorn MH, Bakermans‑Kranenburg MJ, Joëls  M (2015) Complex living conditions impair behavioral inhibition but improve attention in rats. Front Behav Neurosci 24: 357.
• Viola GG, Botton PH, Moreira JD, Ardais AP, Oses JP, Souza DO (2010) In‑ fluence of environmental enrichment on an object recognition task in CF1 mice. Physiol Behav 99: 17–21. 
• Uysal N, Yuksel O, Kizildag S, Yuce Z, Gumus H, Karakilic A, Guvendi G, Koc B, Kandis S, Ates M (2018) Regular aerobic exercise correlates with reduced anxiety and incresed levels of irisin in brain and white adipose tissue. Neurosci Lett 676: 92–97.
• Wang R, Holsinger RMD (2018) Exercise‑induced brain‑derived neuro‑ trophic factor expression: Therapeutic implications for Alzheimer’s de‑ mentia. Ageing Res Rev 48: 109–121.
• Wang XM, Pan W, Xu N, Zhou ZQ, Zhang GF, Shen JC (2019a) Environmental enrichment improves long‑term memory impairment and aberrant syn‑ aptic plasticity by BDNF/TrkB signaling in nerve‑injured mice. Neurosci Lett 16: 93–98.
• Wang XM, Zhang GF, Jia  M, Xie ZM, Yang JJ, Shen JC, Zhou ZQ (2019b) Environmental enrichment improves pain sensitivity, depression‑like phenotype, and memory deficit in mice with neuropathic pain: role of NPAS4. Psychopharmacology (Berl), In press. Zhu SW, Codita A, Bogdanovic N, Hjerling‑Leffler J, Ernfors P, Winblad B, Mo‑ hammed AH (2009) Influence of environmental manipulation on explorato‑ ry behaviour in male BDNF knockout mice. Behav Brain Res 197: 339–346. 
• Zimmermann A,  Stauffacher  M,  Langhans  W, Würbel H (2001) Enrichment‑dependent differences in novelty exploration in rats can be ex‑ plained by habituation. Behav Brain Res 121: 11–20. 

Identyfikatory

DOI

10.21307/ane‑2019‑035