Interneurons are necessary for coordinated activity during reversal learning in orbitofrontal cortex

Biological Psychiatry

Volumn 77, Issue 5, 2015, Pages 454-464

  Bissonette, Gregory B ^a,b,d   Schoenbaum, Geoffrey ^c   Roesch, Matthew R ^d   Powell, Elizabeth M ^a,b  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^d UNIVERSITY OF MARYLAND   (United States)

Author keywords

Autism; Interneuron; OFC; Parvalbumin; Plaur; Reversal learning; Schizophrenia

Indexed keywords

4 AMINOBUTYRIC ACID; PARVALBUMIN; PLAUR PROTEIN, MOUSE; UROKINASE RECEPTOR;

ADULT; ANIMAL EXPERIMENT; ARTICLE; COGNITION; CONTROLLED STUDY; DECISION MAKING; GENE; INTERNEURON; LEARNING; MALE; MOUSE; NONHUMAN; ORBITAL CORTEX; PLAUR GENE; PRIORITY JOURNAL; REWARD; SCHIZOPHRENIA; SINGLE UNIT ACTIVITY; 129 MOUSE; ACTION POTENTIAL; ANIMAL; DISCRIMINATION LEARNING; FRONTAL LOBE; GENETICS; METABOLISM; MICROELECTRODE; NEUROPSYCHOLOGICAL TEST; PHYSIOLOGY; TRANSGENIC MOUSE;

ACTION POTENTIALS; ANIMALS; DECISION MAKING; DISCRIMINATION LEARNING; FRONTAL LOBE; INTERNEURONS; MALE; MICE, 129 STRAIN; MICE, TRANSGENIC; MICROELECTRODES; NEUROPSYCHOLOGICAL TESTS; PARVALBUMINS; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; REVERSAL LEARNING; REWARD;

EID: 84923146057     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2014.07.023     Document Type: Article

References (72)

1. D.A. Lewis, and B. Moghaddam Cognitive dysfunction in schizophrenia: Convergence of gamma-aminobutyric acid and glutamate alterations Arch Neurol 63 2006 1372 1376
2. P. Levitt, K.L. Eagleson, and E.M. Powell Regulation of neocortical interneuron development and the implications for neurodevelopmental disorders Trends Neurosci 27 2004 400 406
3. F.M. Benes, and S. Berretta GABAergic interneurons: Implications for understanding schizophrenia and bipolar disorder Neuropsychopharmacology 25 2001 1 27
4. E. Aronica, S. Redeker, K. Boer, W.G. Spliet, P.C. van Rijen, J.A. Gorter, and D. Troost Inhibitory networks in epilepsy-associated gangliogliomas and in the perilesional epileptic cortex Epilepsy Res 74 2007 33 44
5. Z. Magloczky, and T.F. Freund Impaired and repaired inhibitory circuits in the epileptic human hippocampus Trends Neurosci 28 2005 334 340
6. Y.A. Lawrence, T.L. Kemper, M.L. Bauman, and G.J. Blatt Parvalbumin-, calbindin-, and calretinin-immunoreactive hippocampal interneuron density in autism Acta Neurol Scand 121 2010 99 108
7. J.A. Cardin, M. Carlen, K. Meletis, U. Knoblich, F. Zhang, and K. Deisseroth Driving fast-spiking cells induces gamma rhythm and controls sensory responses Nature 459 2009 663 667
8. T. Sigurdsson, K.L. Stark, M. Karayiorgou, J.A. Gogos, and J.A. Gordon Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia Nature 464 2010 763 767
9. J.E. Belforte, V. Zsiros, E.R. Sklar, Z. Jiang, G. Yu, and Y. Li Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes Nat Neurosci 13 2010 76 83
10. D.B. Campbell, C. Li, J.S. Sutcliffe, A.M. Persico, and P. Levitt Genetic evidence implicating multiple genes in the MET receptor tyrosine kinase pathway in autism spectrum disorder Autism Res 1 2008 159 168
11. P. Roll, S.C. Vernes, N. Bruneau, J. Cillario, M. Ponsole-Lenfant, and A. Massacrier Molecular networks implicated in speech-related disorders: FOXP2 regulates the SRPX2/uPAR complex Hum Mol Genet 19 2010 4848 4860
12. B. Liu, B. Zhang, T. Wang, Q.C. Liang, X.R. Jing, and J. Zheng Increased expression of urokinase-type plasminogen activator receptor in the frontal cortex of patients with intractable frontal lobe epilepsy J Neurosci Res 88 2010 2747 2754
13. B. Royer-Zemmour, M. Ponsole-Lenfant, H. Gara, P. Roll, C. Leveque, and A. Massacrier Epileptic and developmental disorders of the speech cortex: Ligand/receptor interaction of wild-type and mutant SRPX2 with the plasminogen activator receptor uPAR Hum Mol Genet 17 2008 3617 3630
14. E.M. Powell, W.M. Mars, and P. Levitt Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon Neuron 30 2001 79 89
15. E.M. Powell, D.B. Campbell, G.D. Stanwood, C. Davis, J.L. Noebels, and P. Levitt Genetic disruption of cortical interneuron development causes region- and GABA cell type-specific deficits, epilepsy, and behavioral dysfunction J Neurosci 23 2003 622 631
16. K.L. Eagleson, A. Bonnin, and P. Levitt Region- and age-specific deficits in gamma-aminobutyric acidergic neuron development in the telencephalon of the uPAR(-/-) mouse J Comp Neurol 489 2005 449 466
17. G.B. Bissonette, M.H. Bae, T. Suresh, D.E. Jaffe, and E.M. Powell Astrocyte-mediated hepatocyte growth factor/scatter factor supplementation restores GABAergic interneurons and corrects reversal learning deficits in mice J Neurosci 30 2010 2918 2923
18. A. Crider Perseveration in schizophrenia Schizophr Bull 23 1997 63 74
19. J.A. Waltz, and J.M. Gold Probabilistic reversal learning impairments in schizophrenia: Further evidence of orbitofrontal dysfunction Schizophr Res 93 2007 296 303
20. V.C. Leeson, T.W. Robbins, E. Matheson, S.B. Hutton, M.A. Ron, T.R. Barnes, and E.M. Joyce Discrimination learning, reversal, and set-shifting in first-episode schizophrenia: Stability over six years and specific associations with medication type and disorganization syndrome Biol Psychiatry 66 2009 586 593
21. J.L. Silverman, M. Yang, C. Lord, and J.N. Crawley Behavioural phenotyping assays for mouse models of autism Nat Rev Neurosci 11 2010 490 502
22. R. Dias, T.W. Robbins, and A.C. Roberts Primate analogue of the Wisconsin Card Sorting Test: Effects of excitotoxic lesions of the prefrontal cortex in the marmoset Behav Neurosci 110 1996 872 886
23. G. Schoenbaum, S.L. Nugent, M.P. Saddoris, and B. Setlow Orbitofrontal lesions in rats impair reversal but not acquisition of go, no-go odor discriminations Neuroreport 13 2002 885 890
24. K. McAlonan, and V.J. Brown Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat Behav Brain Res 146 2003 97 103
25. M.G. Baxter, and P.G. Browning Two wrongs make a right: Deficits in reversal learning after orbitofrontal damage are improved by amygdala ablation Neuron 54 2007 1 3
26. M.H. Bae, G.B. Bissonette, W.M. Mars, G.K. Michalopoulos, C.L. Achim, D.A. Depireux, and E.M. Powell Hepatocyte growth factor (HGF) modulates GABAergic inhibition and seizure susceptibility Exp Neurol 221 2010 129 135
27. G. Paxinos, and K.B.J. Franklin The Mouse Brain in Stereotaxic Coordinates 2nd ed 2001 Academic Press San Diego
28. G.J. Martins, M. Shahrokh, and E.M. Powell Genetic disruption of Met signaling impairs GABAergic striatal development and cognition Neuroscience 176 2011 199 209
29. G. Colacicco, H. Welzl, H.P. Lipp, and H. Wurbel Attentional set-shifting in mice: Modification of a rat paradigm, and evidence for strain-dependent variation Behav Brain Res 132 2002 95 102
30. G.B. Bissonette, G.J. Martins, T.M. Franz, E.S. Harper, G. Schoenbaum, and E.M. Powell Double dissociation of the effects of medial and orbital prefrontal cortical lesions on attentional and affective shifts in mice J Neurosci 28 2008 11124 11130
31. G. Schoenbaum, and M. Roesch Orbitofrontal cortex, associative learning, and expectancies Neuron 47 2005 1 4
32. G. Schoenbaum, B. Setlow, S.L. Nugent, M.P. Saddoris, and M. Gallagher Lesions of orbitofrontal cortex and basolateral amygdala complex disrupt acquisition of odor-guided discriminations and reversals Learn Mem 10 2003 129 140
33. A.C. Roberts Primate orbitofrontal cortex and adaptive behaviour Trends Cogn Sci 10 2006 83 90
34. H.F. Clarke, J.W. Dalley, H.S. Crofts, T.W. Robbins, and A.C. Roberts Cognitive inflexibility after prefrontal serotonin depletion Science 304 2004 878 880
35. G. van der Plasse, S.S. La Fors, D.T. Meerkerk, R.N. Joosten, H.B. Uylings, and M.G. Feenstra Medial prefrontal serotonin in the rat is involved in goal-directed behaviour when affect guides decision making Psychopharmacology (Berl) 195 2007 435 449
36. G.B. Bissonette, M.H. Bae, T. Suresh, D.E. Jaffe, and E.M. Powell Selective prefrontal cognitive deficits in mice with altered cerebral cortical GABAergic interneurons Behav Brain Res 259 2014 143 151
37. G. Schoenbaum, A.A. Chiba, and M. Gallagher Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning Nat Neurosci 1 1998 155 159
38. G.B. Bissonette, and E.M. Powell Reversal learning and attentional set-shifting in mice Neuropharmacology 62 2012 1168 1174
39. G. Schoenbaum, M.P. Saddoris, and T.A. Stalnaker Reconciling the roles of orbitofrontal cortex in reversal learning and the encoding of outcome expectancies Ann N Y Acad Sci 1121 2007 320 335
40. J. Kim, and M.E. Ragozzino The involvement of the orbitofrontal cortex in learning under changing task contingencies Neurobiol Learn Mem 83 2005 125 133
41. T.A. Stalnaker, Y. Takahashi, M.R. Roesch, and G. Schoenbaum Neural substrates of cognitive inflexibility after chronic cocaine exposure Neuropharmacology 56 suppl 1 2009 63 72
42. K.A. Burke, Y.K. Takahashi, J. Correll, P.L. Brown, and G. Schoenbaum Orbitofrontal inactivation impairs reversal of Pavlovian learning by interfering with 'disinhibition' of responding for previously unrewarded cues Eur J Neurosci 30 2009 1941 1946
43. G. Schoenbaum, B. Setlow, M.P. Saddoris, and M. Gallagher Encoding changes in orbitofrontal cortex in reversal-impaired aged rats J Neurophysiol 95 2006 1509 1517
44. M.E. Ragozzino The contribution of the medial prefrontal cortex, orbitofrontal cortex, and dorsomedial striatum to behavioral flexibility Ann N Y Acad Sci 1121 2007 355 375
45. J.A. Weiler, C. Bellebaum, M. Brune, G. Juckel, and I. Daum Impairment of probabilistic reward-based learning in schizophrenia Neuropsychology 23 2009 571 580
46. J. McKirdy, J.E. Sussmann, J. Hall, S.M. Lawrie, E.C. Johnstone, and A.M. McIntosh Set shifting and reversal learning in patients with bipolar disorder or schizophrenia Psychol Med 39 2009 1289 1293
47. G.K. Murray, F. Cheng, L. Clark, J.H. Barnett, A.D. Blackwell, and P.C. Fletcher Reinforcement and reversal learning in first-episode psychosis Schizophr Bull 34 2008 848 855
48. P. Reed, L. Staytom, S. Stott, and R. Truzoli Comparison of conditioning impairments in children with Down syndrome, autistic spectrum disorders and mental age-matched controls J Intellect Disabil Res 55 2011 988 997
49. R. Dias, T.W. Robbins, and A.C. Roberts Dissociation in prefrontal cortex of affective and attentional shifts Nature 380 1996 69 72
50. V. Boulougouris, J.W. Dalley, and T.W. Robbins Effects of orbitofrontal, infralimbic and prelimbic cortical lesions on serial spatial reversal learning in the rat Behav Brain Res 179 2007 219 228
51. A. Izquierdo, and E.A. Murray Combined unilateral lesions of the amygdala and orbital prefrontal cortex impair affective processing in rhesus monkeys J Neurophysiol 91 2004 2023 2039
52. P.H. Rudebeck, R.C. Saunders, A.T. Prescott, L.S. Chau, and E.A. Murray Prefrontal mechanisms of behavioral flexibility, emotion regulation and value updating Nat Neurosci 16 2013 1140 1145
53. P.H. Rudebeck, and E.A. Murray Amygdala and orbitofrontal cortex lesions differentially influence choices during object reversal learning J Neurosci 28 2008 8338 8343
54. G. Schoenbaum, A.A. Chiba, and M. Gallagher Changes in functional connectivity in orbitofrontal cortex and basolateral amygdala during learning and reversal training J Neurosci 20 2000 5179 5189
55. J.H. Sul, H. Kim, N. Huh, D. Lee, and M.W. Jung Distinct roles of rodent orbitofrontal and medial prefrontal cortex in decision making Neuron 66 2010 449 460
56. D.A. Amodeo, J.H. Jones, J.A. Sweeney, and M.E. Ragozzino Differences in BTBR T+ tf/J and C57BL/6J mice on probabilistic reversal learning and stereotyped behaviors Behav Brain Res 227 2012 64 72
57. M.P. Saddoris, M. Gallagher, and G. Schoenbaum Rapid associative encoding in basolateral amygdala depends on connections with orbitofrontal cortex Neuron 46 2005 321 331
58. A. Racz, A.A. Ponomarenko, E.C. Fuchs, and H. Monyer Augmented hippocampal ripple oscillations in mice with reduced fast excitation onto parvalbumin-positive cells J Neurosci 29 2009 2563 2568
59. A.J. Gruber, E.M. Powell, and P. O'Donnell Cortically activated interneurons shape spatial aspects of cortico-accumbens processing J Neurophysiol 101 2009 1876 1882
60. V.S. Sohal, F. Zhang, O. Yizhar, and K. Deisseroth Parvalbumin neurons and gamma rhythms enhance cortical circuit performance Nature 459 2009 698 702
61. A.R. Delamater The role of the orbitofrontal cortex in sensory-specific encoding of associations in pavlovian and instrumental conditioning Ann N Y Acad Sci 1121 2007 152 173
62. G. Schoenbaum, B. Setlow, M.P. Saddoris, and M. Gallagher Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala Neuron 39 2003 855 867
63. M. Pisa, and J. Cyr Regionally selective roles of the rat's striatum in modality-specific discrimination learning and forelimb reaching Behav Brain Res 37 1990 281 292
64. H.F. Clarke, T.W. Robbins, and A.C. Roberts 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 28 2008 10972 10982
65. R.E. Laughlin, T.L. Grant, R.W. Williams, and J.D. Jentsch Genetic dissection of behavioral flexibility: Reversal learning in mice Biol Psychiatry 69 2011 1109 1116
66. E. van Duuren, J. Lankelma, and C.M. Pennartz Population coding of reward magnitude in the orbitofrontal cortex of the rat J Neurosci 28 2008 8590 8603
67. F.M. Benes, J. McSparren, E.D. Bird, J.P. SanGiovanni, and S.L. Vincent Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients Arch Gen Psychiatry 48 1991 996 1001
68. D.A. Lewis, T. Hashimoto, and D.W. Volk Cortical inhibitory neurons and schizophrenia Nat Rev Neurosci 6 2005 312 324
69. P. Rubin, R. Hemmingsen, S. Holm, S. Moller-Madsen, C. Hertel, U.J. Povlsen, and A. Karle Relationship between brain structure and function in disorders of the schizophrenic spectrum: Single positron emission computerized tomography, computerized tomography and psychopathology of first episodes Acta Psychiatr Scand 90 1994 281 289
70. R. Elliott, P.J. McKenna, T.W. Robbins, and B.J. Sahakian Neuropsychological evidence for frontostriatal dysfunction in schizophrenia Psychol Med 25 1995 619 630
71. J.P. O'Doherty Lights, camembert, action! The role of human orbitofrontal cortex in encoding stimuli, rewards, and choices Ann N Y Acad Sci 1121 2007 254 272
72. E.A. Murray, J.P. O'Doherty, and G. Schoenbaum What we know and do not know about the functions of the orbitofrontal cortex after 20 years of cross-species studies J Neurosci 27 2007 8166 8169