Neural correlates of rules and conflict in medial prefrontal cortex during decision and feedback epochs

Frontiers in Behavioral Neuroscience

Volumn 9, Issue OCT, 2015, Pages

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

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

Conflict; In vivo electrophysiology; MPFC; Rule encoding; Set shifting

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; CELL POPULATION; CONFLICT; CONTROLLED STUDY; DECISION MAKING; EXECUTIVE FUNCTION; FEEDBACK SYSTEM; FIRING RATE; MALE; MEDIAL PREFRONTAL CORTEX; MENTAL TASK; NERVE CELL; NEUROMODULATION; NONHUMAN; OUTCOME ASSESSMENT; PERCEPTIVE DISCRIMINATION; RAT; REWARD; SET SHIFTING TASK; TASK PERFORMANCE;

EID: 84944458081     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2015.00266     Document Type: Article

References (78)

1. Alexander, W. H., and Brown, J. W. (2011). Medial prefrontal cortex as an action-outcome predictor. Nat. Neurosci. 14, 1338-1344. doi: 10.1038/nn.2921
2. Antzoulatos, E. G., and Miller, E. K. (2011). Differences between neural activity in prefrontal cortex and striatum during
3. Bissonette, G. B., Bae, M. H., Suresh, T., Jaffe, D. E., and Powell, E. M. (2014). Prefrontal cognitive deficits in mice with altered cerebral cortical GABAergic interneurons. Behav. Brain Res. 259, 143-151. doi: 10.1016/j.bbr.2013.10.051
4. Bissonette, G. B., Burton, A. C., Gentry, R. N., Goldstein, B. L., Hearn, T. N., Barnett, B. R., et al. (2013). Separate populations of neurons in ventral striatum encode value and motivation. PLoS One 8:e64673. doi: 10.1371/journal.pone.0064673
5. Bissonette, G. B., Martins, G. J., Franz, T. M., Harper, E. S., Schoenbaum, G., and 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. doi: 10.1523/JNEUR0SCI.2820-08.2008
6. Bissonette, G. B., and Roesch, M. R. (2015). Rule encoding in dorsal striatum impacts action selection. Eur. J. Neurosci. doi: 10.1111/ejn.13042 [Epub ahead of print].
7. Bjorklund, A., and Dunnett, S. B. (2007). Dopamine neuron systems in the brain: an update. Trends Neurosci. 30, 194-202. doi: 10.1016/j.tins.2007.03.006
8. Block, A. E., Dhanji, H., Thompson-Tardif, S. F., and Floresco, S. B. (2007). Thalamic-prefrontal cortical-ventral striatal circuitry mediates dissociable components of strategy set shifting. Cereb. Cortex 17, 1625-1636. doi: 10.1093/cercor/bhl073
9. Boettiger, C. A., and D’Esposito, M. (2005). Frontal networks for learning and executing arbitrary stimulus-response associations. J. Neurosci. 25, 2723-2732. doi: 10.1523/jneurosci.3697-04.2005
10. Brigman, J. L., Daut, R. A., Wright, T., Gunduz-Cinar, O., Graybeal, C., Davis, M. I., et al. (2013). GluN2B in corticostriatal circuits governs choice learning and choice shifting. Nat. Neurosci. 16, 1101-1110. doi: 10.1038/nn.3457
11. Brown, J. W., and Braver, T. S. (2005). Learned predictions of error likelihood in the anterior cingulate cortex. Science 307, 1118-1121. doi: 10.1126/science.1105783
12. Bryden, D. W., Burton, A. C., Kashtelyan, V., Barnett, B. R., and Roesch, M. R. (2012). Response inhibition signals and miscoding of direction in dorsomedial striatum. Front. Integr. Neurosci. 6:69. doi: 10.3389/fnint.2012.00069
13. Bryden, D. W., Johnson, E. E., Tobia, S. C., Kashtelyan, V., and Roesch, M. R. (2011). Attention for learning signals in anterior cingulate cortex. J. Neurosci. 31, 18266-18274. doi: 10.1523/JNEUR0SCI.4715-11.2011
14. Bunge, S. A., Kahn, I., Wallis, J. D., Miller, E. K., and Wagner, A. D. (2003). Neural circuits subserving the retrieval and maintenance of abstract rules. J. Neurophysiol. 90, 3419-3428. doi: 10.1152/jn.00910.2002
15. Burton, A. C., Bissonette, G. B., Lichtenberg, N. T., Kashtelyan, V., and Roesch, M. R. (2013). Ventral striatum lesions enhance stimulus and response encoding in dorsal striatum. Biol. Psychiatry 75, 132-139. doi: 10.1016/j.biopsych.2013.05.023
16. Carr, D. B., and Sesack, S. R. (1996). Hippocampal afferents to the rat prefrontal cortex: synaptic targets and relation to dopamine terminals. J. Comp. Neurol. 369, 1-15. doi: 10.1002/(sici)1096-9861(19960520)369:1<1::aid-cne1>3.0.co;2-7
17. Cho, K. K., Hoch, R., Lee, A. T., Patel, T., Rubenstein, J. L., and Sohal, V. S. (2015). Gamma rhythms link prefrontal interneuron dysfunction with cognitive inflexibility in dlx5/6(+/-) mice. Neuron 85, 1332-1343. doi: 10.1016/j.neuron.2015.02.019
18. Colacicco, G., Welzl, H., Lipp, H. P., and 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. doi: 10.1016/s0166-4328(01)00391-6
19. Cools, R., Brouwer, W. H., de Jong, R., and Slooff, C. (2000). Flexibility, inhibition and planning: frontal dysfunctioning in schizophrenia. Brain Cogn. 43, 108-112.
20. Corbit, L. H., and Balleine, B. W. (2003). The role of prelimbic cortex in instrumental conditioning. Behav. Brain Res. 146, 145-157. doi: 10.1016/j.bbr.2003.09.023
21. Cromer, J. A., Roy, J. E., and Miller, E. K. (2010). Representation of multiple, independent categories in the primate prefrontal cortex. Neuron 66, 796-807. doi: 10.1016/j.neuron.2010.05.005
22. Dalton, G. L., Ma, L. M., Phillips, A. G., and Floresco, S. B. (2011). Blockade of NMDA GluN2B receptors selectively impairs behavioral flexibility but not initial discrimination learning. Psychopharmacology (Berl) 216, 525-535. doi: 10.1007/s00213-011-2246-z
23. Dias, R., Robbins, T. W., and Roberts, A. C. (1996a). Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380, 69-72. doi: 10.1038/380069a0
24. Dias, R., Robbins, T. W., and Roberts, A. C. (1996b). Primate analogue of the wisconsin card sortingtest: effects of excitotoxic lesions of the prefrontal cortex in the marmoset. Behav. Neurosci. 110, 872-886. doi: 10.1037/0735-7044.110.5.872
25. Dirnberger, G., and Jahanshahi, M. (2013). Executive dysfunction in parkinson’s disease: areview. J. Neuropsychol. 7, 193-224. doi: 10.1111/jnp.12028
26. Durstewitz, D., Vittoz, N. M., Floresco, S. B., and Seamans, J. K. (2010). Abrupt transitions between prefrontal neural ensemble states accompany behavioral transitions during rule learning. Neuron 66, 438-448. doi: 10.1016/j.neuron.2010.03.029
27. Elliott, R., McKenna, P. J., Robbins, T. W., and Sahakian, B. J. (1995). Neuropsychological evidence for frontostriatal dysfunction in schizophrenia. Psychol. Med. 25, 619-630. doi: 10.1017/s0033291700033523
28. Floresco, S. B., Block, A. E., and 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. doi: 10.1016/j.bbr.2008.02.008
29. Floresco, S. B., Magyar, O., Ghods-Sharifi, S., Vexelman, C., and Tse, M. T. (2006). Multiple dopamine receptor subtypes in the medial prefrontal cortex of the rat regulate set-shifting. Neuropsychopharmacology 31, 297-309. doi: 10.1038/sj.npp.1300825
30. Gabbott, P. L., Warner, T. A., Jays, P. R., Salway, P., and Busby, S. J. (2005). Prefrontal cortex in the rat: projections to subcortical autonomic, motor and limbic centers. J. Comp. Neurol. 492, 145-177. doi: 10.1002/cne.20738
31. Gauntlett-Gilbert, J., Roberts, R. C., and Brown, V. J. (1999). Mechanisms underlying attentional set-shifting in parkinson’s disease. Neuropsychologia 37, 605-616. doi: 10.1016/s0028-3932(98)00049-9
32. Glimcher, P. W. (2011). Understanding dopamine and reinforcement learning: the dopamine reward prediction error hypothesis. Proc. Natl. Acad. Sci. U S A 108(Suppl. 3), 15647-15654. doi: 10.1073/pnas.1014269108
33. Gold, J. M., Hahn, B., Strauss, G. P., and Waltz, J. A. (2009). Turning it upside down: areas of preserved cognitive function in schizophrenia. Neuropsychol. Rev. 19,294-311. doi: 10.1007/s11065-009-9098-x
34. Gold, J. M., Waltz, J. A., Prentice, K. J., Morris, S. E., and Heerey, E. A. (2008). Reward processing in schizophrenia: a deficit in the representation of value. Schizophr. Bull. 34, 835-847. doi: 10.1093/schbul/sbn068
35. Harlow, H. F. (1949). The formation of learning sets. Psychol. Rev. 56, 51-65. doi: 10.1037/h0062474
36. Hayden, B. Y., Heilbronner, S. R., Pearson, J. M., and Platt, M. L. (2011). Surprise signals in anterior cingulate cortex: neuronal encoding of unsigned reward prediction errors driving adjustment in behavior. J. Neurosci. 31, 4178-4187. doi: 10.1523/JNEUROSCI.4652-10.2011
37. Hoover, W. B., and Vertes, R. P. (2007).Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct 212, 149-179. doi: 10.1007/s00429-007-0150-4
38. Horst, N. K., and Laubach, M. (2009). The role of rat dorsomedial prefrontal cortex in spatial working memory. Neuroscience 164, 444-456. doi: 10.1016/j.neuroscience.2009.08.004
39. Horst, N. K., and Laubach, M. (2012). Working with memory: evidence for a role for the medial prefrontal cortex in performance monitoring during spatial delayed alternation. J. Neurophysiol. 108, 3276-3288. doi: 10.1152/jn.01192.2011
40. Kesner, R. P., Hunt, M. E., Williams, J. M., and Long, J. M. (1996). Prefrontal cortex and working memory for spatial response, spatial location and visual object information in the rat. Cereb. Cortex 6,311-318. doi: 10.1093/cercor/6.2.311
41. Laubach, M., Caetano, M. S., and Narayanan, N. S. (2015). Mistakes were made: neural mechanisms for the adaptive control of action initiation by the medial prefrontal cortex. J. Physiol. Paris 109, 104-117. doi: 10.1016/j.jphysparis.2014.12.001
42. Lyvers, M., and Yakimoff, M. (2003). Neuropsychological correlates of opioid dependence and withdrawal. Addict. Behav. 28, 605-611. doi: 10.1016/s0306-4603(01)00253-2
43. Marquardt, K., Saha, M., Mishina, M., Young, J. W., and Brigman, J. L. (2014). Loss of GluN2A-containing NMDA receptors impairs extra-dimensional set-shifting. Genes BrainBehav. 13, 611-617. doi: 10.1111/gbb.12156
44. Miller, H. L., Ragozzino, M. E., Cook, E. H., Sweeney, J. A., and 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. doi: 10.1007/s10803-014-2244-1
45. Monchi, O., Petrides, M., Doyon, J., Postuma, R. B., Worsley, K., and Dagher, A. (2004). Neural bases of set-shifting deficits in parkinson’s disease. J. Neurosci. 24, 702-710. doi: 10.1523/jneurosci.4860-03.2004
46. Muhammad, R., Wallis, J. D., and Miller, E. K. (2006). A comparison of abstract rules in the prefrontal cortex, premotor cortex, inferior temporal cortex and striatum. J. Cogn. Neurosci. 18, 974-989. doi: 10.1162/jocn.2006.18.6.974
47. Narayanan, N. S., and Laubach, M. (2009). Methods for studying functional interactions among neuronal populations. Methods Mol. Biol. 489, 135-165. doi: 10.1007/978-1-59745-543-5_7
48. Nelson, H. E. (1976). A modified card sorting test sensitive to frontal lobe defects. Cortex 12, 313-324. doi: 10.1016/s0010-9452(76)80035-4
49. Nieder, A., Freedman, D. J., and Miller, E. K. (2002). Representation ofthe quantity ofvisual items in the primate prefrontal cortex. Science 297, 1708-1711. doi: 10.1126/science.1072493
50. Oliveira, F. T., Mcdonald, J. J., and Goodman, D. (2007). Performance monitoring in the anterior cingulate is not all error related: expectancy deviation and the representation of action-outcome associations. J. Cogn. Neurosci. 19, 1994-2004. doi: 10.1162/jocn.2007.19.12.1994
51. Pantelis, C., Barber, F. Z., Barnes, T. R., Nelson, H. E., Owen, A. M., and Robbins, T. W. (1999). Comparison of set-shifting ability in patients with chronic schizophrenia and frontal lobe damage. Schizophr. Res. 37, 251-270. doi: 10.1016/s0920-9964(98)00156-x
52. Paxinos, G., and Watson, C. (2004). The Rat Brain in Stereotaxic Coordinates-The New Coronal Set. Amsterdam: Elsevier Science.
53. Prentice, K. J., Gold, J. M., and Buchanan, R. W. (2008). The wisconsin card sorting impairment in schizophrenia is evident in the first four trials. Schizophr. Res. 106, 81-87. doi: 10.1016/j.schres.2007.07.015
54. Ragozzino, M. E. (2002). The effects of dopamine D(1) receptor blockade in the prelimbic-infralimbic areas on behavioral flexibility. Learn. Mem. 9, 18-28. doi: 10.1101/lm.45802
55. Ragozzino, M. E. (2007). The contribution of the medial prefrontal cortex, orbitofrontal cortex and dorsomedial striatum to behavioral flexibility. Ann. N. Y. Acad. Sci. 1121, 355-375. doi: 10.1196/annals.1401.013
56. Ragozzino, M. E., Adams, S., and Kesner, R. P. (1998). Differential involvement of the dorsal anterior cingulate and prelimbic-infralimbic areas of the rodent prefrontal cortex in spatial working memory. Behav. Neurosci. 112, 293-303. doi: 10.1037//0735-7044.112.2.293
57. Ragozzino, M. E., Detrick, S., and Kesner, R. P. (1999a). Involvement of the prelimbic-infralimbic areas of the rodent prefrontal cortex in behavioral flexibility for place and response learning. J. Neurosci. 19, 4585-4594.
58. Ragozzino, M. E., Wilcox, C., Raso, M., and Kesner, R. P. (1999b). Involvement of rodent prefrontal cortex subregions in strategy switching. Behav. Neurosci. 113, 32-41. doi: 10.1037//0735-7044.113.1.32
59. Rainer, G., Rao, S. C., and Miller, E. K. (1999). Prospective coding for objects in primate prefrontal cortex. J. Neurosci. 19, 5493-5505.
60. Roesch, M. R., and Bryden, D. W. (2011). Impact of size and delay on neural activity in the rat limbic corticostriatal system. Front. Neurosci. 5:130. doi: 10.3389/fnins.2011.00130
61. Roesch, M. R., Calu, D. J., Esber, G. R., and Schoenbaum, G. (2010). All that glitters... dissociating attention and outcome expectancy from prediction errors signals. J. Neurophysiol. 104, 587-595. doi: 10.1152/jn.00173.2010
62. Roesch, M. R., Calu, D. J., and Schoenbaum, G. (2007). Dopamine neurons encode the better option in rats deciding between differently delayed or sized rewards. Nat. Neurosci. 10, 1615-1624. doi: 10.1038/nn2013
63. Roy, J. E., Riesenhuber, M., Poggio, T., and Miller, E. K. (2010). Prefrontal cortex activity during flexible categorization. J. Neurosci. 30, 8519-8528. doi: 10.1523/jneurosci.4837-09.2010
64. Schoenbaum, G., and Roesch, M. (2005). Orbitofrontal cortex, associative learning and expectancies. Neuron 47, 633-636. doi: 10.1016/j.neuron.2005.07.018
65. Schultz, W., and Dickinson, A. (2000). Neuronal coding of prediction errors. Annu. Rev. Neurosci. 23, 473-500. doi: 10.1146/annurev.neuro.23.1.473
66. Seamans, J. K., Floresco, S. B., and Phillips, A. G. (1995). Functional differences between the prelimbic and anterior cingulate regions of the rat prefrontal cortex. Behav. Neurosci. 109, 1063-1073.doi: 10.1037//0735-7044.109.6.1063
67. Shamay-Tsoory, S. G., Tomer, R., Goldsher, D., Berger, B. D., and Aharon-Peretz, J. (2004). Impairment in cognitive and affective empathy in patients with brain lesions: anatomical and cognitive correlates. J. Clin. Exp. Neuropsychol. 26, 1113-1127. doi: 10.1080/13803390490515531
68. Stalnaker, T. A., Calhoon, G. G., Ogawa, M., Roesch, M. R., and Schoenbaum, G. (2012). Reward prediction error signaling in posterior dorsomedial striatum is action specific. J. Neurosci. 32, 10296-10305. doi: 10.1523/jneurosci.0832-12.2012
69. Stefani, M. R., Groth, K., and Moghaddam, B. (2003). Glutamate receptors in the rat medial prefrontal cortex regulate set-shifting ability. Behav. Neurosci. 117, 728-737. doi: 10.1037/0735-7044.117.4.728
70. Stefani, M. R., and 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. doi: 10.1523/jneurosci.1656-06.2006
71. Strauss, G. P., Robinson, B. M., Waltz, J. A., Frank, M. J., Kasanova, Z., Herbener, D.S., et al. (2011). Patients with schizophrenia demonstrate inconsistent preferencejudgments for affective and nonaffective stimuli. Schizophr. Bull. 37, 1295-1304. doi: 10.1093/schbul/sbq047
72. Tait, D. S., Brown, V. J., Farovik, A., Theobald, D. E., Dalley, J. W., and Robbins, T. W. (2007). Lesions of the dorsal noradrenergic bundle impair attentional set-shifting in the rat. Eur. J. Neurosci. 25, 3719-3724. doi: 10.1111/j.1460-9568.2007.05612.x
73. Totah, N. K., Jackson, M. E., and Moghaddam, B. (2012). Preparatory attention relies on dynamic interactions between prelimbic cortex and anterior cingulate cortex. Cereb. Cortex 23, 729-738. doi: 10.1093/cercor/bhs057
74. Totah, N. K., Kim, Y. B., Homayoun, H., and Moghaddam, B. (2009). Anterior cingulate neurons represent errors and preparatory attention within the same behavioral sequence. J. Neurosci. 29, 6418-6426. doi: 10.1523/jneurosci.1142-09.2009
75. Vertes, R. P. (2004). Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51, 32-58. doi: 10.1002/syn.10279
76. Waelti, P., Dickinson, A., and Schultz, W. (2001). Dopamine responses comply with basic assumptions of formal learning theory. Nature 412, 43-48. doi: 10.1038/35083500
77. Wallis, J. D., Anderson, K. C., and Miller, E. K. (2001). Single neurons in prefrontal cortex encode abstract rules. Nature 411, 953-956. doi: 10.1038/35082081
78. White, I. M., and Wise, S. P. (1999). Rule-dependent neuronal activity in the prefrontal cortex. Exp. Brain Res. 126, 315-335. doi: 10.1007/s002210050740