Cited by 14Memory and Neural MechanismsNeural and Behavioral Psychology StudiesStress Responses and Cortisol

Complex living conditions impair behavioral inhibition but improve attention in rats.

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van der Veen, Rixt, Kentrop, Jiska, van der Tas, Liza, Loi, Manila, van IJzendoorn, Marinus H., Bakermans-Kranenburg, Marian J., Joëls, Marian·2015·Frontiers in Behavioral Neuroscience

Abstract

Rapid adaptation to changes, while maintaining a certain level of behavioral inhibition is an important feature in every day functioning. How environmental context and challenges in life can impact on the development of this quality is still unknown. In the present study, we examined the effect of a complex rearing environment during adolescence on attention and behavioral inhibition in adult male rats. We also tested whether these effects were affected by an adverse early life challenge, maternal deprivation (MD). We found that animals that were raised in large, two floor Marlau(TM) cages, together with 10 conspecifics, showed improved attention, but impaired behavioral inhibition in the 5-choice serial reaction time task. The early life challenge of 24 h MD on postnatal day 3 led to a decline in bodyweight during adolescence, but did not by itself influence responses in the 5-choice task in adulthood, nor did it moderate the effects of complex housing. Our data suggest that a complex rearing environment leads to a faster adaptation to changes in the environment, but at the cost of lower behavioral inhibition.

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  1. Baarendse P. J. Counotte D. S. O’Donnell P. Vanderschuren L. J. (2013). Early social experience is critical for the development of cognitive control and dopamine modulation of prefrontal cortex function. Neuropsychopharmacology 38 1485– 1494. 10.1038/npp.2013.47 23403694 PMC3682143 · DOI · Paper page
  2. Bagot R. C. van Hasselt F. N. Champagne D. L. Meaney M. J. Krugers H. J. Joels M. (2009). Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus. Neurobiol. Learn. Mem. 92 292– 300. 10.1016/j.nlm.2009.03.004 19292996 · DOI · Paper page
  3. Bari A. Dalley J. W. Robbins T. W. (2008). The application of the 5-choice serial reaction time task for the assessment of visual attentional processes and impulse control in rats. Nat Protoc. 3 759– 767. 10.1038/nprot.2008.41 18451784 · DOI · Paper page
  4. Burke N. N. Llorente R. Marco E. M. Tong K. Finn D. P. Viveros M. P. (2013). Maternal deprivation is associated with sex-depend ent alterations in nociceptive behavior and neuroinflammatory mediators in the rat following peripheral nerve injury. J. Pain 14 1173– 1184. 10.1016/j.jpain.2013.05.003 23850096 · DOI
  5. Champagne D. L. Bagot R. C. van Hasselt F. Ramakers G. Meaney M. J. de Kloet E. R. (2008). Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J. Neurosci. 28 6037– 6045. 10.1523/jneurosci.0526-08.2008 18524909 PMC6670331 · DOI · Paper page
  6. Claessens S. E. Daskalakis N. P. van der Veen R. Oitzl M. S. de Kloet E. R. Champagne D. L. (2011). Development of individual differences in stress responsiveness: an overview of factors mediating the outcome of early life experiences. Psychopharmacology (Berl.) 214 141– 154. 10.1007/s00213-010-2118-y 21165737 PMC3045508 · DOI
  7. Colorado R. A. Shumake J. Conejo N. M. Gonzalez-Pardo H. Gonzalez-Lima F. (2006). Effects of maternal separation, early handling, and standard facility rearing on orienting and impulsive behavior of adolescent rats. Behav. Process. 71 51– 58. 10.1016/j.beproc.2005.09.007 16242858 · DOI
  8. Comeau W. L. Winstanley C. A. Weinberg J. (2014). Prenatal alcohol exposure and adolescent stress - unmasking persistent attentional deficits in rats. Eur. J. Neurosci. 40 3078– 3095. 10.1111/ejn.12671 25059261 PMC4189965 · DOI
  9. Dalley J. W. Everitt B. J. Robbins T. W. (2011). Impulsivity, compulsivity, and top-down cognitive control. Neuron 69 680– 694. 10.1016/j.neuron.2011.01.020 21338879 · DOI · Paper page
  10. Dalley J. W. Fryer T. D. Brichard L. Robinson E. S. Theobald D. E. Laane K. (2007). Nucleus accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement. Science 315 1267– 1270. 10.1126/science.1137073 17332411 PMC1892797 · DOI · Paper page
  11. Ellenbroek B. A. van den Kroonenberg P. T. Cools A. R. (1998). The effects of an early stressful life event on sensorimotor gating in adult rats. Schizophr. Res. 30 251– 260. 10.1016/S0920-9964(97)00149-7 9589519 · DOI
  12. Fares R. P. Belmeguenai A. Sanchez P. E. Kouchi H. Y. Bodennec J. Morales A. (2013). Standardized environmental enrichment supports enhanced brain plasticity in healthy rats and prevents cognitive impairment in epileptic rats. PLoS ONE 8: e53888 10.1371/journal.pone.0053888 PMC3544705 23342033 · DOI
  13. Fergusson D. M. Boden J. M. Horwood L. J. (2013). Childhood self-control and adult outcomes: results from a 30-year longitudinal study. J. Am. Acad. Child Adolesc. Psychiatry 52 709– 717e701. 10.1016/j.jaac.2013.04.008 23800484 · DOI · Paper page
  14. Haller J. Harold G. Sandi C. Neumann I. D. (2014). Effects of adverse early-life events on aggression and anti-social behaviours in animals and humans. J. Neuroendocrinol. 26 724– 738. 10.1111/jne.12182 25059307 · DOI
  15. Halperin J. M. Healey D. M. (2011). The influences of environmental enrichment, cognitive enhancement, and physical exercise on brain development: can we alter the developmental trajectory of ADHD? Neurosci. Biobehav. Rev. 35 621– 634. 10.1016/j.neubiorev.2010.07.006 20691725 PMC3008505 · DOI · Paper page
  16. Leggio M. G. Mandolesi L. Federico F. Spirito F. Ricci B. Gelfo F. (2005). Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav. Brain Res. 163 78– 90. 10.1016/j.bbr.2005.04.009 15913801 · DOI · Paper page
  17. Lehmann J. Pryce C. R. Feldon J. (2000). Lack of effect of an early stressful life event on sensorimotor gating in adult rats. Schizophr. Res. 41 365– 371. 10.1016/S0920-9964(99)00080-8 10708346 · DOI
  18. Levine S. (2005). Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology 30 939– 946. 10.1016/j.psyneuen.2005.03.013 15958281 · DOI · Paper page
  19. Marco E. M. Llorente R. Lopez-Gallardo M. Mela V. Llorente-Berzal A. Prada C. (2015). The maternal deprivation animal model revisited. Neurosci. Biobehav. Rev. 51 151– 163. 10.1016/j.neubiorev.2015.01.015 25616179 · DOI · Paper page
  20. Moffitt T. E. Arseneault L. Belsky D. Dickson N. Hancox R. J. Harrington H. (2011). A gradient of childhood self-control predicts health, wealth, and public safety. Proc. Natl. Acad. Sci. U.S.A. 108 2693– 2698. 10.1073/pnas.1010076108 21262822 PMC3041102 · DOI · Paper page
  21. O’Donnell K. A. Gaudreau H. Colalillo S. Steiner M. Atkinson L. Moss E. (2014). The maternal adversity, vulnerability and neurodevelopment project: theory and methodology. Can. J. Psychiatry 59 497– 508. 25565695 PMC4168812
  22. Oomen C. A. Soeters H. Audureau N. Vermunt L. van Hasselt F. N. Manders E. M. (2010). Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood. J. Neurosci. 30 6635– 6645. 10.1523/jneurosci.0247-10.2010 20463226 PMC6632559 · DOI
  23. Perry J. L. Stairs D. J. Bardo M. T. (2008). Impulsive choice and environmental enrichment: effects of d-amphetamine and methylphenidate. Behav. Brain Res. 193 48– 54. 10.1016/j.bbr.2008.04.019 18534693 PMC2681296 · DOI
  24. Petersen S. E. Posner M. I. (2012). The attention system of the human brain: 20 years after. Annu. Rev. Neurosci. 35 73– 89. 10.1146/annurev-neuro-062111-150525 22524787 PMC3413263 · DOI · Paper page
  25. Pryce C. R. Feldon J. (2003). Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms. Neurosci. Biobehav. Rev. 27 57– 71. 10.1016/S0149-7634(03)00009-5 12732223 · DOI
  26. Robbins T. W. (2002). The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology (Berl.) 163 362– 380. 10.1007/s00213-002-1154-7 12373437 · DOI · Paper page
  27. Robinson T. E. Yager L. M. Cogan E. S. Saunders B. T. (2014). On the motivational properties of reward cues: Individual differences. Neuropharmacology 76(Pt B), 450– 459. 10.1016/j.neuropharm.2013.05.040 23748094 PMC3796005 · DOI
  28. Rosenzweig M. R. Bennett E. L. (1996). Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav. Brain Res. 78 57– 65. 10.1016/0166-4328(95)00216-2 8793038 · DOI · Paper page
  29. Rots N. Y. de Jong J. Workel J. O. Levine S. Cools A. R. De Kloet E. R. (1996). Neonatal maternally deprived rats have as adults elevated basal pituitary-adrenal activity and enhanced susceptibility to apomorphine. J. Neuroendocrinol. 8 501– 506. 10.1046/j.1365-2826.1996.04843.x 8843018 · DOI
  30. Solinas M. Thiriet N. Chauvet C. Jaber M. (2010). Prevention and treatment of drug addiction by environmental enrichment. Prog. Neurobiol. 92 572– 592. 10.1016/j.pneurobio.2010.08.002 20713127 · DOI
  31. Spivey J. M. Shumake J. Colorado R. A. Conejo-Jimenez N. Gonzalez-Pardo H. Gonzalez-Lima F. (2009). Adolescent female rats are more resistant than males to the effects of early stress on prefrontal cortex and impulsive behavior. Dev. Psychobiol. 51 277– 288. 10.1002/dev.20362 19125421 PMC2754836 · DOI
  32. Stairs D. J. Bardo M. T. (2009). Neurobehavioral effects of environmental enrichment and drug abuse vulnerability. Pharmacol. Biochem. Behav. 92 377– 382. 10.1016/j.pbb.2009.01.016 19463254 PMC2687322 · DOI
  33. Sullivan R. M. Brake W. G. (2003). What the rodent prefrontal cortex can teach us about attention-deficit/hyperactivity disorder: the critical role of early developmental events on prefrontal function. Behav. Brain Res. 146 43– 55. 10.1016/j.bbr.2003.09.015 14643458 · DOI
  34. Tunstall B. J. Kearns D. N. (2015). Sign-tracking predicts increased choice of cocaine over food in rats. Behav. Brain Res. 281 222– 228. 10.1016/j.bbr.2014.12.034 25541036 PMC4305489 · DOI
  35. Van den Buuse M. Garner B. Koch M. (2003). Neurodevelopmental animal models of schizophrenia: effects on prepulse inhibition. Curr. Mol. Med. 3 459– 471. 10.2174/1566524033479627 12942999 · DOI
  36. van Oers H. J. de Kloet E. R. Levine S. (1997). Persistent, but paradoxical, effects on HPA regulation of infants maternally deprived at different ages. Stress 1 249– 262. 9787249
  37. van Praag H. Kempermann G. Gage F. H. (2000). Neural consequences of environmental enrichment. Nat. Rev. Neurosci. 1 191– 198. 10.1038/35044558 11257907 · DOI · Paper page
  38. Winstanley C. A. Eagle D. M. Robbins T. W. (2006). Behavioral models of impulsivity in relation to ADHD: translation between clinical and preclinical studies. Clin. Psychol. Rev. 26 379– 395. 10.1016/j.cpr.2006.01.001 16504359 PMC1892795 · DOI
  39. Wurbel H. (2001). Ideal homes? Housing effects on rodent brain and behaviour. Trends Neurosci. 24 207– 211. 10.1016/S0166-2236(00)01718-5 11250003 · DOI · Paper page
  40. Zimmermann A. Stauffacher M. Langhans W. Wurbel H. (2001). Enrichment-dependent differences in novelty exploration in rats can be explained by habituation. Behav. Brain Res. 121 11– 20. 10.1016/S0166-4328(00)00377-6 11275280 · DOI · Paper page

Cited by

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Authors
van der Veen, R., Kentrop, J., van der Tas, L., Loi, M., van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., & Joëls, M.
Affiliations
University Medical Center Utrecht (NL)
Venue
Frontiers in Behavioral Neuroscience
Published
2015-12-24
Volume
9
Pages
357-357
ISSN
1662-5153 (ISSN-L)
OpenAlex
W2224839333
Cited by
14
References
7
Citations by year
2026: 1 · 2023: 1 · 2022: 3 · 2021: 3 · 2020: 4 · 2018: 1 · 2016: 1
FWCI
0.40
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Leiden Repository (Leiden University) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
  • Data Archiving and Networked Services (DANS) (submittedVersion)
Funders
Gravitation program of the Dutch Ministry of Education, Culture, and Science and the Netherlands Organization for Scientific Research (NWO grant number 024.001.003)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords
behavioral inhibition, attention, maternal deprivation, childhood adversity, adolescence, residential environment, 5-choice serial reaction time task, rats, environmental enrichment, adaptation to change

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