Early-life maternal separation and social isolation produce an increase in impulsive action but not impulsive choice

Behavioral Neuroscience

Volumn 125, Issue 4, 2011, Pages 481-491

  Lovic, Vedran ^a,b   Keen, Darren ^a   Fletcher, Paul J ^a   Fleming, Alison S ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Development; Impulsivity; Isolation; Maternal; Social

Indexed keywords

ANALYTIC METHOD; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; ARTIFICIAL REARING ON IMPULSIVE ACTION; ARTIFICIAL REARING ON IMPULSIVE CHOICE; CONTROLLED STUDY; DELAY DISCOUNTING; DEVELOPMENTAL STAGE; EMOTION; FEMALE; IMPULSIVENESS; LICKING; MALE; MATERNAL DEPRIVATION; NONHUMAN; OUTCOME ASSESSMENT; RAT; REINFORCEMENT; RESPONSE TIME; SEX RATIO; SOCIAL ISOLATION; TASK PERFORMANCE;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CHOICE BEHAVIOR; CONDITIONING, OPERANT; FEMALE; FOOD DEPRIVATION; IMPULSIVE BEHAVIOR; MALE; MATERNAL DEPRIVATION; RATS; RATS, SPRAGUE-DAWLEY; REINFORCEMENT (PSYCHOLOGY); REINFORCEMENT SCHEDULE; SOCIAL ISOLATION; TIME FACTORS;

EID: 79960965314     PISSN: 07357044     EISSN: 19390084     Source Type: Journal    
DOI: 10.1037/a0024367     Document Type: Article

References (53)

1. Akbari, E. M., Budin, R., Chatterjee, D., Maheu, M., & Fleming, A. S. (2010, September). Maternal deprivation produces alterations in the androgen and dopamine systems and results in deficits in masculine sexual behavior. Partial reversal with maternal 'licking-like' stimulation during the deprivation period. Paper presented at the Parental Brain conference, Edinburgh, Scotland.
2. Akbari E.M., Budin R., Parada M., Fleming A.S. The effects of early isolation on sexual behaviour and c-fos expression in naïve male Long-Evans rats. Developmental Psychobiology 2008, 50:298-306.
3. Belin D., Mar A.C., Dalley J.W., Robbins T.W., Everitt B.J. High impulsivity predicts the switch to compulsive cocaine-taking. Science 2008, 320(5881):1352-1355.
4. Brake W.G., Zhang T.Y., Diorio J., Meaney M.J., Gratton A. Influence of early postnatal rearing conditions on mesocorticolimbic dopamine and behavioural responses to psychostimulants and stressors in adult rats. European Journal of Neuroscience 2004, 19:1863-1874.
5. Burton C., Lovic V., Fleming A.S. Early adversity alters attention and locomotion in adult Sprague-Dawley rats. Behavioural Neuroscience 2006, 120:665-675.
6. Cardinal R.N. Neural systems implicated in delayed and probabilistic reinforcement. Neural Networks 2006, 19:1277-1301.
7. Cardinal R.N., Parkinson J.A., Hall J., Everitt B.J. Emotion and motivation: The role of the amygdala, ventral striatum, and prefrontal cortex. Neuroscience and Biobehavioral Reviews 2002, 26:321-352.
8. Cardinal R.N., Pennicott D.R., Sugathapala C.L., Robbins T.W., Everitt B.J. Impulsive choice induced in rats by lesions of the nucleus accumbens. Science 2001, 292(5526):2499-2501.
9. Chugani H.T., Behem M.E., Muzik O., Juhasz C., Nagy F., Chugani D.C. Local brain functional activity following early deprivation: A study of postinstitutionalized Romanian orphans. NeuroImage 2001, 14:1290-1301.
10. Cirulli F., Berry A., Alleva E. Early disruptions of the mother-infant relationship: Effects on brain plasticity and implications for psychopathology. Neuroscience and Biobehavioural Reviews 2003, 27:73-82.
11. Cole B.J., Robbins T.W. Amphetamine impairs the discriminative performance of rats with dorsal noradrenergic bundle lesions on a 5-choice serial reaction time task: New evidence for central dopaminergic-noradrenergic interactions. Psychopharmacology 1987, 91:458-466.
12. Dalley J.W., Everitt B.J., Robbins T.W. Impulsivity, compulsivity and top-down cognitive control. Neuron 2011, 69:680-694.
13. Dellu-Hagedorn F. Relationship between impulsivity, hyperactivity and working memory: A differential analysis in the rat. Behavioural and Brain Functions 2006, 28:2-10.
14. de Wit H. Impulsivity as a determinant and consequence of drug use: A review of underlying processes. Addiction Biology 2009, 14:22-31.
15. Enoch M.A., Hodgkinson C.A., Yuan Q., Shen P.H., Goldman D., Roy A. The influence of GABARA2, childhood trauma, and their interaction on alcohol, heroin, and cocaine dependence. Biological Psychiatry 2010, 67:20-27.
16. Evenden J.L. The pharmacology of impulsive behaviour in rats, II: The effects of amphetamine, haloperidol, imipramine, chlordiazepoxide and other drugs on fixed consecutive number schedules (FCN 8 and FCN 32). Psychopharmacology 1998, 138:283-294.
17. Evenden J.L. Varieties of impulsivity. Psychopharmacology 1999, 146:348-361.
18. Fletcher P.J. Effects of combined or separate 5, 7-dihydroxytryptamine lesions of the dorsal and median raphe nuclei on responding maintained by a DRL 20s schedule of food reinforcement. Brain Research 1995, 675(1-2):45-54.
19. Fletcher, P. J., Rizos, Z., Noble, K., & Higgins, G. A. (in press). Impulsive action induced by amphetamine, cocaine and MK801 is reduced by 5-HT(2C) receptor stimulation and 5-HT(2A) receptor blockade. Neuropharmacology. Advance online publication. doi: 10.1016/j.neuropharm.2011.02.025.
20. Gonzalez A., Lovic V., Ward G.R., Wainwright P.E., Fleming A.S. Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behaviour and emotionality in female rats. Developmental Psychobiology 2001, 38:11-42.
21. Hall F.S. Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioural consequences. Critical Reviews in Neurobiology 1998, 12:129-169.
22. Hall F.S., Wilkinson L.S., Humby T., Robbins T.W. Maternal deprivation of neonatal rats produces enduring changes in dopamine function. Synapse 1999, 32:37-43.
23. Hellemans K.G., Nobrega J.N., Olmstead M.C. Early environmental experience alters baseline and ethanol-induced cognitive impulsivity: Relationship to forebrain 5- HT1A receptor binding. Behavioural Brain Research 2005, 159:207-220.
24. Ho M.-Y., Mobini S., Chiang T.-J., Bradshaw C.M., Szabadi E. Theory and method in the quantitative analysis of "impulsive choice" behaviour: Implications for psychopharmacology. Psychopharmacology 1999, 146:362-373.
25. Hofer M.A. Early relationships as regulators of infant physiology and behaviour. Acta Paediatrica 1994, 397:9-18.
26. Jentch J.D., Taylor J.R. Impulsivity resulting from frontostriatal dysfunction in drug abuse: Implications for the control of behaviour by reward-related stimuli. Psychopharmacology 1999, 146:373-390.
27. Kaffman A., Meaney M.J. Neurodevelopmental sequelae of postnatal maternal care in rodents: Clinical and research implications of molecular insights. Journal of Child Psychology and Psychiatry 2007, 48:224-244.
28. Koss M.P., Yuan N.P., Dightman D., Prince R.J., Polacca M., Sanderson B., Goldman D. Adverse childhood exposures and alcohol dependence among seven Native American tribes. American Journal of Preventive Medicine 2003, 25:238-244.
29. Kuhn C.M., Schanberg S.M. Response to maternal separation: Mechanisms and mediators. International Journal of Developmental Neuroscience 1998, 16:261-270.
30. Lévy F., Melo A.I., Galef B.G., Madden M., Fleming A.S. Complete maternal deprivation affects social, but not spatial, learning in adult rats. Developmental Psychobiology 2003, 43:177-191.
31. Lomanowska A.M., Lovic V., Rankine M.J., Mooney S.J., Robinson T.E., Kraemer G.W. Inadequate early social experience increases the incentive salience of reward-related cues in adulthood. Behavioural Brain Research 2011, 220:91-99.
32. Lovibond P.F. Facilitation of instrumental behavior by a Pavlovian appetitive conditioned stimulus. Journal of Experimental Psychology: Animal Behavior Processes 1983, 9:225-247.
33. Lovic V., Fleming A.S. Artificially-reared female rats show reduced prepulse inhibition and deficits in the attentional set shifting task-reversal of effects with maternal-like licking stimulation. Behavioural Brain Research 2004, 148:209-219.
34. Lovic V., Fleming A.S., Fletcher P.J. Early life tactile stimulation changes adult rat responsiveness to amphetamine. Pharmacology, Biochemistry and Behaviour 2006, 84:497-503.
35. Lovic V., Palombo D.J., Fleming A.S. Impulsive rats are less maternal. Developmental Psychobiology 2011, 53:13-22.
36. Lovic, V., Saunders, B. T., Yager, L. M., & Robinson, T. E. (in press). Rats prone to attribute incentive salience to reward cues are also prone to impulsive action. Behavioural Brain Research. Advance online publication. doi: 10.1016/j.bbr.2011.04.006.
37. Matthews K., Dalley J.W., Matthews C., Tsai T.H., Robbins T.W. Periodic maternal separation of neonatal rats produces region- and gender- specific effects on biogenic amine content in postmortem adult brain. Synapse 2001, 40:1-10.
38. Meaney M.J., Diorio J., Francis D., Weaver S., Yau J., Chapman K., Seckl J.R. Postnatal handling increases the expression of cAMP-inducible transcription factors in the rat hippocampus: The effects of thyroid hormone and serotonin. Journal of Neuroscience 2000, 20:3935-3936.
39. Melo A.I., Lovic V., Gonzalez, Madden M., Sinopoli K., Fleming A.S. Maternal and littermate deprivation disrupts maternal behaviour and social-learning of food preference in adulthood: Tactile stimulation, nest odor, and social rearing prevent these effects. Developmental Psychobiology 2006, 48:209-219.
40. Moore C.L., Moralli G.A. Mother rats interact differently with male and female offspring. Journal of Comparative Physiological Psychology 1979, 93:677-684.
41. Olmstead M.C. Animal models of drug addiction: Where do we go from here?. Quarterly Journal of Experimental Psychology (Colchester) 2006, 59:625-653.
42. Pattij T., Vanderschuren L.J. The neuropharmacology of impulsive behaviour. Trends in Pharmacological Science 2008, 29(4):192-199.
43. Perry J.L., Carroll M.E. The role of impulsive behaviour in drug abuse. Psychopharmacology 2008, 200:1-26.
44. Peterson J.D., Wolf M.E., White F.J. Impaired DRL 30 performance during amphetamine withdrawal. Behavioural Brain Research 2003, 143:101-108.
45. Pryce C.R., Feldon J. Long-term neurobehavioural impact of the postnatal environment in rats: Manipulations, effects and mediating mechanisms. Neuroscience and Biobehavioural Reviews 2003, 27(1-2):57-71.
46. Reynolds B., de Wit H., Richards J.B. Delay of gratification and delay discounting in rats. Behavioural Processes 2002, 59:157-168.
47. Robbins T.W. The 5-choice serial reaction time task: Behavioural pharmacology and functional neurochemistry. Psychopharmacology 2002, 163:363-380.
48. Uslaner J.M., Robinson T.E. Subthalamic nucleus lesion increase impulsive action and decrease impulsive choice-Mediation by enhanced incentive motivation?. European Journal of Neuroscience 2006, 24:2345-2354.
49. Widom C.S., Weiler B.L., Cottler L.B. Childhood victimization and drug abuse: A comparison of prospective and retrospective findings. Journal of Consulting and Clinical Psychology 1999, 67:867-880.
50. Wilsnack S.C., Vogeltanz N.D., Klassen A.D., Harris T.R. Childhood sexual abuse and women's substance abuse: National survey findings. Journal of Studies On Alcohol 1997, 58(3):264-271.
51. Winstanley C.A., Dalley J.W., Theobald D.E., Robbins T.W. Global 5-HT depletion attenuates the ability of amphetamine to decrease impulsive choice on a delay-discounting task in rats. Psychopharmacology 2003, 170:320-331.
52. Winstanley C.A., Dalley J.W., Theobald D.E., Robbins T.W. Fractioning impulsivity: Contrasting effects of central 5-HT depletion on different measures of impulsive behaviour. Neuropsychopharmacology 2004, 29:1331-1343.
53. Winstanley C.A., Theobald D.E., Cardinal R.N., Robbins T.W. Contrasting roles of basolateral amygdala and orbitofrontal cortex in impulsive choice. Journal of Neuroscience 2004, 24:4718-4722.