Rule encoding in dorsal striatum impacts action selection

European Journal of Neuroscience

Volumn 42, Issue 8, 2015, Pages 2555-2567

  Bissonette, Gregory B ^a   Roesch, Matthew R ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

Attentional set shifting; Cognitive flexibility; Medial dorsal striatum; Rat; Single unit

Indexed keywords

ACTION SELECTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CONTROL; COGNITION; CONTROLLED STUDY; DORSOMEDIAL STRIATUM; MALE; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RAT; REWARD; RULE ENCODING; TASK PERFORMANCE; ACTION POTENTIAL; ANIMAL; CORPUS STRIATUM; DRUG EFFECTS; ELECTRODE IMPLANT; EXECUTIVE FUNCTION; INDWELLING CATHETER; LONG EVANS RAT; NERVE CELL; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE;

4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; 4 AMINOBUTYRIC ACID B RECEPTOR STIMULATING AGENT; BACLOFEN; MUSCIMOL;

ACTION POTENTIALS; ANIMALS; BACLOFEN; CATHETERS, INDWELLING; CORPUS STRIATUM; ELECTRODES, IMPLANTED; EXECUTIVE FUNCTION; GABA-A RECEPTOR AGONISTS; GABA-B RECEPTOR AGONISTS; MALE; MUSCIMOL; NEURONS; PSYCHOMOTOR PERFORMANCE; RATS, LONG-EVANS; REWARD;

EID: 84944511317     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.13042     Document Type: Article

References (71)

1. Antzoulatos, E.G. & Miller, E.K. (2011) Differences between neural activity in prefrontal cortex and striatum during learning of novel abstract categories. Neuron, 71, 243-249.
2. Baker, P.M. & Ragozzino, M.E. (2014) Contralateral disconnection of the rat prelimbic cortex and dorsomedial striatum impairs cue-guided behavioral switching. Learn. Memory, 21, 368-379.
3. Balleine, B.W. & O'Doherty, J.P. (2010) Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology, 35, 48-69.
4. Balleine, B.W., Delgado, M.R. & Hikosaka, O. (2007) The role of the dorsal striatum in reward and decision-making. J. Neurosci., 27, 8161-8165.
5. Balleine, B.W., Liljeholm, M. & Ostlund, S.B. (2009) The integrative function of the basal ganglia in instrumental conditioning. Behav. Brain Res., 199, 43-52.
6. Birrell, J.M. & Brown, V.J. (2000) Medial frontal cortex mediates perceptual attentional set shifting in the rat. J. Neurosci., 20, 4320-4324.
7. Bissonette, G.B., Martins, G.J., Franz, T.M., Harper, E.S., Schoenbaum, G. & Powell, E.M. (2008) Double dissociation of the effects of medial and orbital prefrontal cortical lesions on attentional and affective shifts in mice. J. Neurosci., 28, 11124-11130.
8. Bissonette, G.B., Burton, A.C., Gentry, R.N., Goldstein, B.L., Hearn, T.N., Barnett, B.R., Kashtelyan, V. & Roesch, M.R. (2013a) Separate populations of neurons in ventral striatum encode value and motivation. PLoS One, 8, e64673.
9. Bissonette, G.B., Powell, E.M. & Roesch, M.R. (2013b) Neural structures underlying set-shifting: roles of medial prefrontal cortex and anterior cingulate cortex. Behav. Brain Res., 250, 91-101.
10. Bissonette, G.B., Bae, M.H., Suresh, T., Jaffe, D.E. & Powell, E.M. (2014) Prefrontal cognitive deficits in mice with altered cerebral cortical GABAergic interneurons. Behav. Brain Res., 259, 143-151.
11. Bissonette, G.B., Schoenbaum, G., Roesch, M.R. & Powell, E.M. (2015) Interneurons are necessary for coordinated activity during reversal learning in orbitofrontal cortex. Biol. Psychiat., 77, 454-464.
12. Botvinick, M.M., Braver, T.S., Barch, D.M., Carter, C.S. & Cohen, J.D. (2001) Conflict monitoring and cognitive control. Psychol. Rev., 108, 624-652.
13. Botvinick, M.M., Cohen, J.D. & Carter, C.S. (2004) Conflict monitoring and anterior cingulate cortex: an update. Trends Cogn. Sci., 8, 539-546.
14. Brown, J.W. & Braver, T.S. (2008) A computational model of risk, conflict, and individual difference effects in the anterior cingulate cortex. Brain Res., 1202, 99-108.
15. Bryden, D.W., Burton, A.C., Kashtelyan, V., Barnett, B.R. & Roesch, M.R. (2012) Response inhibition signals and miscoding of direction in dorsomedial striatum. Front. Integr. Neurosci., 6, 69.
16. Burton, A.C., Bissonette, G.B., Lichtenberg, N.T., Kashtelyan, V. & Roesch, M.R. (2014) Ventral striatum lesions enhance stimulus and response encoding in dorsal striatum. Biol. Psychiat., 75, 132-139.
17. Cohen, M.X. & Frank, M.J. (2009) Neurocomputational models of basal ganglia function in learning, memory and choice. Behav. Brain Res., 199, 141-156.
18. Colacicco, G., Welzl, H., Lipp, H.P. & Wurbel, H. (2002) Attentional set-shifting in mice: modification of a rat paradigm, and evidence for strain-dependent variation. Behav. Brain Res., 132, 95-102.
19. Collins, A.G. & Frank, M.J. (2013) Cognitive control over learning: creating, clustering, and generalizing task-set structure. Psychol. Rev., 120, 190-229.
20. Cools, R. (2011) Dopaminergic control of the striatum for high-level cognition. Curr. Opin. Neurobiol., 21, 402-407.
21. Cools, R., Brouwer, W.H., de Jong, R. & Slooff, C. (2000) Flexibility, inhibition, and planning: frontal dysfunctioning in schizophrenia. Brain Cognition, 43, 108-112.
22. Corbett, B.A., Constantine, L.J., Hendren, R., Rocke, D. & Ozonoff, S. (2009) Examining executive functioning in children with autism spectrum disorder, attention deficit hyperactivity disorder and typical development. Psychiat. Res., 166, 210-222.
23. Cromer, J.A., Roy, J.E. & Miller, E.K. (2010) Representation of multiple, independent categories in the primate prefrontal cortex. Neuron, 66, 796-807.
24. Dias, R., Robbins, T.W. & Roberts, A.C. (1996a) Dissociation in prefrontal cortex of affective and attentional shifts. Nature, 380, 69-72.
25. Dias, R., Robbins, T.W. & Roberts, A.C. (1996b) Primate analogue of the Wisconsin Card Sorting Test: effects of excitotoxic lesions of the prefrontal cortex in the marmoset. Behav. Neurosci., 110, 872-886.
26. Dirnberger, G. & Jahanshahi, M. (2013) Executive dysfunction in Parkinson's disease: a review. J. Neuropsyc., 7, 193-224.
27. Durstewitz, D., Vittoz, N.M., Floresco, S.B. & Seamans, J.K. (2010) Abrupt transitions between prefrontal neural ensemble states accompany behavioral transitions during rule learning. Neuron, 66, 438-448.
28. Elliott, R., McKenna, P.J., Robbins, T.W. & Sahakian, B.J. (1995) Neuropsychological evidence for frontostriatal dysfunction in schizophrenia. Psychol. Med., 25, 619-630.
29. Floresco, S.B., Ghods-Sharifi, S., Vexelman, C. & Magyar, O. (2006) Dissociable roles for the nucleus accumbens core and shell in regulating set shifting. J. Neurosci., 26, 2449-2457.
30. Floresco, S.B., Block, A.E. & Tse, M.T. (2008) Inactivation of the medial prefrontal cortex of the rat impairs strategy set-shifting, but not reversal learning, using a novel, automated procedure. Behav. Brain Res., 190, 85-96.
31. Gabbott, P.L., Warner, T.A., Jays, P.R., Salway, P. & Busby, S.J. (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J. Comp. Neurol., 492, 145-177.
32. Gauntlett-Gilbert, J., Roberts, R.C. & Brown, V.J. (1999) Mechanisms underlying attentional set-shifting in Parkinson's disease. Neuropsychologia, 37, 605-616.
33. Gold, J.M., Waltz, J.A., Prentice, K.J., Morris, S.E. & Heerey, E.A. (2008) Reward processing in schizophrenia: a deficit in the representation of value. Schizophrenia Bull., 34, 835-847.
34. Gold, J.M., Hahn, B., Strauss, G.P. & Waltz, J.A. (2009) Turning it upside down: areas of preserved cognitive function in schizophrenia. Neuropsychol. Rev., 19, 294-311.
35. Hilario, M., Holloway, T., Jin, X. & Costa, R.M. (2012) Different dorsal striatum circuits mediate action discrimination and action generalization. Eur. J. Neuorsci., 35, 1105-1114.
36. Jones, J.L., Esber, G.R., McDannald, M.A., Gruber, A.J., Hernandez, A., Mirenzi, A. & Schoenbaum, G. (2012) Orbitofrontal cortex supports behavior and learning using inferred but not cached values. Science, 338, 953-956.
37. Kimchi, E.Y. & Laubach, M. (2009) Dynamic encoding of action selection by the medial striatum. J. Neurosci., 29, 3148-3159.
38. Lyvers, M. & Yakimoff, M. (2003) Neuropsychological correlates of opioid dependence and withdrawal. Addict. Behav., 28, 605-611.
39. Markett, S., Montag, C., Walter, N.T., Plieger, T. & Reuter, M. (2011) On the molecular genetics of flexibility: the case of task-switching, inhibitory control and genetic variants. Cogn. Affect. Behav. Ne., 11, 644-651.
40. Mayer, A.R., Teshiba, T.M., Franco, A.R., Ling, J., Shane, M.S., Stephen, J.M. & Jung, R.E. (2012) Modeling conflict and error in the medial frontal cortex. Hum. Brain Mapp., 33, 2843-2855.
41. van der Meer, M.A., Johnson, A., Schmitzer-Torbert, N.C. & Redish, A.D. (2010) Triple dissociation of information processing in dorsal striatum, ventral striatum, and hippocampus on a learned spatial decision task. Neuron, 67, 25-32.
42. Miller, E.K. & Cohen, J.D. (2001) An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci., 24, 167-202.
43. Miller, H.L., Ragozzino, M.E., Cook, E.H., Sweeney, J.A. & Mosconi, M.W. (2015) Cognitive set shifting deficits and their relationship to repetitive behaviors in autism spectrum disorder. J. Autism Dev. Disord., 45, 805-815.
44. Moghaddam, B. & Homayoun, H. (2008) Divergent plasticity of prefrontal cortex networks. Neuropsychopharmacology, 33, 42-55.
45. Monchi, O., Petrides, M., Doyon, J., Postuma, R.B., Worsley, K. & Dagher, A. (2004) Neural bases of set-shifting deficits in Parkinson's disease. J. Neurosci., 24, 702-710.
46. Muhammad, R., Wallis, J.D. & Miller, E.K. (2006) A comparison of abstract rules in the prefrontal cortex, premotor cortex, inferior temporal cortex, and striatum. J. Cognitive Neurosci., 18, 974-989.
47. Murray, E.A., Bussey, T.J. & Wise, S.P. (2000) Role of prefrontal cortex in a network for arbitrary visuomotor mapping. Exp. Brain Res., 133, 114-129.
48. Nieder, A., Freedman, D.J. & Miller, E.K. (2002) Representation of the quantity of visual items in the primate prefrontal cortex. Science, 297, 1708-1711.
49. Pantelis, C., Barber, F.Z., Barnes, T.R., Nelson, H.E., Owen, A.M. & Robbins, T.W. (1999) Comparison of set-shifting ability in patients with chronic schizophrenia and frontal lobe damage. Schizophr. Res., 37, 251-270.
50. Pardo, J.V., Pardo, P.J., Janer, K.W. & Raichle, M.E. (1990) The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. Proc. Natl. Acad. Sci. USA, 87, 256-259.
51. Parsegian, A., Glen, W.B. Jr., Lavin, A. & See, R.E. (2011) Methamphetamine self-administration produces attentional set-shifting deficits and alters prefrontal cortical neurophysiology in rats. Biol. Psychiat., 69, 253-259.
52. Pasupathy, A. & Miller, E.K. (2005) Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature, 433, 873-876.
53. Paxinos, G. & Watson, C. (2004) The Rat Brain in Stereotaxic Coordinates - The New Coronal Set. Elsevier Science, Amsterdam.
54. Ragozzino, M.E., Ragozzino, K.E., Mizumori, S.J. & Kesner, R.P. (2002) Role of the dorsomedial striatum in behavioral flexibility for response and visual cue discrimination learning. Behav. Neurosci., 116, 105-115.
55. Rich, E.L. & Shapiro, M.L. (2007) Prelimbic/infralimbic inactivation impairs memory for multiple task switches, but not flexible selection of familiar tasks. J. Neurosci., 27, 4747-4755.
56. Ritchie, T. & Noble, E.P. (2003) Association of seven polymorphisms of the D2 dopamine receptor gene with brain receptor-binding characteristics. Neurochem. Res., 28, 73-82.
57. Rodgers, C.C. & DeWeese, M.R. (2014) Neural correlates of task switching in prefrontal cortex and primary auditory cortex in a novel stimulus selection task for rodents. Neuron, 82, 1157-1170.
58. Roy, J.E., Riesenhuber, M., Poggio, T. & Miller, E.K. (2010) Prefrontal cortex activity during flexible categorization. J. Neurosci., 30, 8519-8528.
59. Rushworth, M.F., Kennerley, S.W. & Walton, M.E. (2005) Cognitive neuroscience: resolving conflict in and over the medial frontal cortex. Curr. Biol., 15, R54-R56.
60. Schoenbaum, G. & Roesch, M. (2005) Orbitofrontal cortex, associative learning, and expectancies. Neuron, 47, 633-636.
61. Shamay-Tsoory, S.G., Tomer, R., Goldsher, D., Berger, B.D. & Aharon-Peretz, J. (2004) Impairment in cognitive and affective empathy in patients with brain lesions: anatomical and cognitive correlates. J. Clin. Exp. Neuropsyc., 26, 1113-1127.
62. Stefani, M.R. & Moghaddam, B. (2006) Rule learning and reward contingency are associated with dissociable patterns of dopamine activation in the rat prefrontal cortex, nucleus accumbens, and dorsal striatum. J. Neurosci., 26, 8810-8818.
63. Stefani, M.R., Groth, K. & Moghaddam, B. (2003) Glutamate receptors in the rat medial prefrontal cortex regulate set-shifting ability. Behav. Neurosci., 117, 728-737.
64. Stelzel, C., Basten, U., Montag, C., Reuter, M. & Fiebach, C.J. (2010) Frontostriatal involvement in task switching depends on genetic differences in d2 receptor density. J. Neurosci., 30, 14205-14212.
65. Strauss, G.P., Robinson, B.M., Waltz, J.A., Frank, M.J., Kasanova, Z., Herbener, E.S. & Gold, J.M. (2011) Patients with schizophrenia demonstrate inconsistent preference judgments for affective and nonaffective stimuli. Schizophrenia Bull., 37, 1295-1304.
66. Takarae, Y., Minshew, N.J., Luna, B. & Sweeney, J.A. (2007) Atypical involvement of frontostriatal systems during sensorimotor control in autism. Psychiat. Res., 156, 117-127.
67. Thorn, C.A., Atallah, H., Howe, M. & Graybiel, A.M. (2010) Differential dynamics of activity changes in dorsolateral and dorsomedial striatal loops during learning. Neuron, 66, 781-795.
68. Toni, I., Rushworth, M.F. & Passingham, R.E. (2001) Neural correlates of visuomotor associations. Spatial rules compared with arbitrary rules. Exp. Brain Res., 141, 359-369.
69. Wallis, J.D. & Miller, E.K. (2003) From rule to response: neuronal processes in the premotor and prefrontal cortex. J. Neurophysiol., 90, 1790-1806.
70. Wallis, J.D., Anderson, K.C. & Miller, E.K. (2001) Single neurons in prefrontal cortex encode abstract rules. Nature, 411, 953-956.
71. Yerys, B.E., Wallace, G.L., Harrison, B., Celano, M.J., Giedd, J.N. & Kenworthy, L.E. (2009) Set-shifting in children with autism spectrum disorders: reversal shifting deficits on the Intradimensional/Extradimensional Shift Test correlate with repetitive behaviors. Autism, 13, 523-538.