Selective lesions of the dorsomedial striatum impair serial spatial reversal learning in rats

Behavioural Brain Research

Volumn 210, Issue 1, 2010, Pages 74-83

  Castane Anna A ^a,b   Theobald, David E H ^a   Robbins, Trevor W ^a  

^a UK   (United Kingdom)

^b INST D INVESTIGACIONS B   (Spain)

Author keywords

Behavioural flexibility; Discrimination; Excitotoxic lesion; Learning; Nucleus accumbens; Perseveration; Spatial reversal learning; Striatum

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; CONTROLLED STUDY; CORPUS STRIATUM; LEARNING DISORDER; LOCOMOTION; MALE; MENTAL PERFORMANCE; NONHUMAN; NUCLEUS ACCUMBENS; PERSEVERATION; PRIORITY JOURNAL; RAT; REINFORCEMENT; SPATIAL DISCRIMINATION; VISUAL DISCRIMINATION;

ANIMALS; CORPUS STRIATUM; DISCRIMINATION (PSYCHOLOGY); EATING; EXTINCTION, PSYCHOLOGICAL; IBOTENIC ACID; MALE; MEMORY; MOTOR ACTIVITY; NEUROPSYCHOLOGICAL TESTS; NEUROTOXINS; NUCLEUS ACCUMBENS; QUINOLINIC ACID; RATS; REVERSAL LEARNING; SPACE PERCEPTION; TIME FACTORS;

EID: 77949571493     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2010.02.017     Document Type: Article

References (43)

1. Abi-Dargham A., van de Giessen E., Slifstein M., Kegeles L.S., Laruelle M. Baseline and amphetamine-stimulated dopamine activity are related in drug-naïve schizophrenic subjects. Biol Psychiatry 2009, 65:1091-1093.
2. Annett L.E., McGregor A., Robbins T.W. The effects of ibotenic acid lesions of the nucleus accumbens on spatial learning and extinction in the rat. Behav Brain Res 1989, 31:231-242.
3. Balleine B., Killcross S. Effects of ibotenic acid lesions of the nucleus accumbens on instrumental action. Behav Brain Res 1994, 65:181-193.
4. Balleine B.W., Liljeholm M., Ostlund S.B. The integrative function of the basal ganglia in instrumental conditioning. Behav Brain Res 2009, 199:43-52.
5. Birrell J.M., Brown V.J. Medial frontal cortex mediates perceptual attentional set-shifting in the rat. J Neurosci 2000, 20:4320-4324.
6. Boulougouris V., Castañé A., Robbins T.W. Dopamine D2/D3 receptor agonist quinpirole impairs spatial reversal learning in rats: investigation of D3 receptor involvement in persistent behavior. Psychopharmacology 2009, 202:611-620.
7. Boulougouris V., Dalley J.W., Robbins T.W. Effects of orbitofrontal, infralimbic and prelimbic cortical lesions on serial spatial reversal learning in the rat. Behav Brain Res 2007, 179:219-228.
8. Burk J.A., Mair R.G. Effects of dorsal and ventral striatal lesions on delayed matching trained with retractable levers. Behav Brain Res 2001, 122:67-78.
9. Chudasama Y., Robbins T.W. Dissociable contributions of the orbitofrontal and infralimbic cortex to pavlovian autoshaping and discrimination reversal learning: further evidence for the functional heterogeneity of the rodent frontal cortex. J Neurosci 2003, 23:8771-8780.
10. Clarke H.F., Robbins T.W., Roberts A.C. Lesions of the medial striatum in monkeys produce perseverative impairments during reversal learning similar to those produced by lesions of the orbitofrontal cortex. J Neurosci 2008, 28:10972-10982.
11. Cools R., Lewis S.J., Clark L., Barker R.A., Robbins T.W. L-DOPA disrupts activity in the nucleus accumbens during reversal learning in Parkinson's disease. Neuropsychopharmacology 2007, 32:180-189.
12. Di Ciano P., Robbins T.W., Everitt B.J. Differential effects of nucleus accumbens core, shell, or dorsal striatal inactivations on the persistence, reacquisition, or reinstatement of responding for a drug-paired conditioned reinforcer. Neuropsychopharmacology 2008, 33:1413-1425.
13. Dias R., Robbins T.W., Roberts A.C. Dissociation in prefrontal cortex of affective and attentional shifts. Nature 1996, 380:69-72.
14. Divac I., Rosvold H.E., Szwarcbart M.K. Behavioral effects of selective ablation of the caudate nucleus. J Comp Physiol Psychol 1967, 63:184-190.
15. Eagle D.M., Humby T., Dunnett S.B., Robbins T.W. Effects of regional striatal lesions on motor, motivational, and executive aspects of progressive-ratio performance in rats. Behav Neurosci 1999, 113:718-731.
16. Eagle D.M., Humby T., Howman M., Reid-Henry A., Dunnett S.B., Robbins T.W. Differential effects of ventral and regional dorsal striatal lesions on sucrose drinking and positive and negative contrast in rats. Psychobiology 1999, 27:267-276.
17. Floresco S.B., Ghods-Sharifi S., Vexelman C., Magyar O. Dissociable roles for the nucleus accumbens core and shell in regulating set shifting. J Neurosci 2006, 26:2449-2457.
18. Floresco S.B., Zhang Y., Enomoto T. Neural circuits subserving behavioral flexibility and their relevance to schizophrenia. Behav Brain Res 2009, 204:396-409.
19. Guillin O., Abi-Dargham A., Laruelle M. Neurobiology of dopamine in schizophrenia. Int Rev Neurobiol 2007, 78:1-39.
20. Haluk D.M., Floresco S.B. Ventral striatal dopamine modulation of different forms of behavioral flexibility. Neuropsychopharmacology 2009, 34:2041-2052.
21. Hornak J., O'Doherty J., Bramham J., Rolls E.T., Morris R.G., Bullock P.R., et al. Reward-related reversal learning after surgical excisions in orbito-frontal or dorsolateral prefrontal cortex in humans. J Cogn Neurosci 2004, 16:463-478.
22. Izquierdo A., Suda R.K., Murray E.A. Bilateral orbital prefrontal cortex lesions in rhesus monkeys disrupt choices guided by both reward value and reward contingency. J Neurosci 2004, 24:7540-7548.
23. Jones B., Mishkin M. Limbic lesions and the problem of stimulus-reinforcement associations. Exp Neurol 1972, 36:362-377.
24. Kolb B. Studies on the caudate-putamen and the dorsomedial thalamic nucleus of the rat: implications for mammalian frontal-lobe functions. Physiol Behav 1977, 18:237-244.
25. Lee B., Groman S., London E.D., Jentsch J.D. Dopamine D2/D3 receptors play a specific role in the reversal of a learned visual discrimination in monkeys. Neuropsychopharmacology 2007, 32:2125-2134.
26. McAlonan K., Brown V.J. Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behav Brain Res 2003, 146:97-103.
27. Murphy E.R., Robinson E.S., Theobald D.E., Dalley J.W., Robbins T.W. Contrasting effects of selective lesions of nucleus accumbens core or shell on inhibitory control and amphetamine-induced impulsive behaviour. Eur J Neurosci 2008, 28:353-363.
28. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, New York.
29. Ragozzino M.E., Detrick S., Kesner R.P. Involvement of the prelimbic-infralimbic areas of the rodent prefrontal cortex in behavioral flexibility for place and response learning. J Neurosci 1999, 19:4585-4594.
30. Ragozzino M.E., Jih J., Tzavos A. Involvement of the dorsomedial striatum in behavioral flexibility: role of muscarinic cholinergic receptors. Brain Res 2002, 953:205-214.
31. Ragozzino M.E., Mohler E.G., Prior M., Palencia C.A., Rozman S. Acetylcholine activity in selective striatal regions supports behavioral flexibility. Neurobiol Learn Mem 2009, 91:13-22.
32. Ragozzino M.E., Ragozzino K.E., Mizumori S.J., Kesner R.P. Role of the dorsomedial striatum in behavioral flexibility for response and visual cue discrimination learning. Behav Neurosci 2002, 116:105-115.
33. Ragozzino M.E. The contribution of the medial prefrontal cortex, orbitofrontal cortex, and dorsomedial striatum to behavioral flexibility. Ann NY Acad Sci 2007, 1121:355-375.
34. Reading P.J., Dunnett S.B., Robbins T.W. Dissociable roles of the ventral, medial and lateral striatum on the acquisition and performance of a complex visual stimulus-response habit. Behav Brain Res 1991, 45:147-161.
35. Reading P.J., Dunnett S.B. The effects of excitotoxic lesions of the nucleus accumbens on a matching to position task. Behav Brain Res 1991, 46:17-29.
36. Roberts A.C., Tomic D.L., Parkinson C.H., Roeling T.A., Cutter D.J., Robbins T.W., et al. Forebrain connectivity of the prefrontal cortex in the marmoset monkey (Callithrix jacchus): an anterograde and retrograde tract-tracing study. J Comp Neurol 2007, 502:86-112.
37. Schilman E.A., Uylings H.B., Galis-de Graaf Y., Joel D., Groenewegen H.J. The orbital cortex in rats topographically projects to central parts of the caudate-putamen complex. Neurosci Lett 2008, 432:40-45.
38. Schoenbaum G., Setlow B. Lesions of nucleus accumbens disrupt learning about aversive outcomes. J Neurosci 2003, 23:9833-9841.
39. Stern C.E., Passingham R.E. The nucleus accumbens in monkeys (Macaca fascicularis). III. Reversal learning. Exp Brain Res 1995, 106:239-247.
40. Taghzouti K., Louilot A., Herman J.P., Le Moal M., Simon H. Alternation behavior, spatial discrimination, and reversal disturbances following 6-hydroxydopamine lesions in the nucleus accumbens of the rat. Behav Neural Biol 1985, 44:354-363.
41. Tzavos A., Jih J., Ragozzino M.E. Differential effects of M1 muscarinic receptor blockade and nicotinic receptor blockade in the dorsomedial striatum on response reversal learning. Behav Brain Res 2004, 154:245-253.
42. Walker S.C., Robbins T.W., Roberts A.C. Differential contributions of dopamine and serotonin to orbitofrontal cortex function in the marmoset. Cereb Cortex 2009, 19:889-898.
43. Yin H.H., Knowlton B.J., Balleine B.W. Inactivation of dorsolateral striatum enhances sensitivity to changes in the action-outcome contingency in instrumental conditioning. Behav Brain Res 2006, 166:189-196.