Parvalbumin-positive interneurons of the prefrontal cortex support working memory and cognitive flexibility

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Murray, Andrew J ^a,b   Woloszynowska Fraser, Marta U ^a   Ansel Bollepalli, Laura ^a,c   Cole, Katy L H ^a   Foggetti, Angelica ^a,c   Crouch, Barry ^a   Riedel, Gernot ^a   Wulff, Peer ^a,c  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c UNIVERSITY OF KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHETAMINE; METALLOPROTEINASE; PARVALBUMIN; TETANUS TOXIN; ZINC-ENDOPEPTIDASE, TETANUS NEUROTOXIN;

ANIMAL; ANIMAL BEHAVIOR; COGNITION; CYTOLOGY; DRUG EFFECTS; FEMALE; INTERNEURON; MALE; METABOLISM; PREFRONTAL CORTEX; SHORT TERM MEMORY; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; SYNAPTIC TRANSMISSION;

AMPHETAMINE; ANIMALS; BEHAVIOR, ANIMAL; COGNITION; FEMALE; INTERNEURONS; MALE; MEMORY, SHORT-TERM; METALLOENDOPEPTIDASES; PARVALBUMINS; PREFRONTAL CORTEX; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; SYNAPTIC TRANSMISSION; TETANUS TOXIN;

EID: 84948459081     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep16778     Document Type: Article

References (73)

1. Allen, P. et al. Transition to psychosis associated with prefrontal and subcortical dysfunction in ultra high-risk individuals. Schizophr Bull 38, 1268-1276 (2012).
2. Baas, D. et al. Evidence of altered cortical and amygdala activation during social decision-making in schizophrenia. NeuroImage 40, 719-727 (2008).
3. Meyer-Lindenberg, A. et al. Reduced prefrontal activity predicts exaggerated striatal dopaminergic function in schizophrenia. Nat. Neurosci. 5, 267-271 (2002).
4. Weinberger, D. R. & Berman, K. F. Prefrontal function in schizophrenia: confounds and controversies. Philos. Trans. R. Soc. Lond. B Biol. Sci. 351, 1495-1503 (1996).
5. Wolkin, A. et al. Negative symptoms and hypofrontality in chronic schizophrenia. Arch. Gen. Psychiatry 49, 959-965 (1992).
6. Benes, F. M., Vincent, S. L., Marie, A. & Khan, Y. Up-regulation of GABAA receptor binding on neurons of the prefrontal cortex in schizophrenic subjects. Neuroscience 75, 1021-1031 (1996).
7. Hanada, S., Mita, T., Nishino, N. & Tanaka, C. [3H]muscimol binding sites increased in autopsied brains of chronic schizophrenics. Life Sci. 40, 259-266 (1987).
8. Lewis, D. A., Hashimoto, T. & Volk, D. W. Cortical inhibitory neurons and schizophrenia. Nat. Rev. Neurosci. 6, 312-324 (2005).
9. Guidotti, A. et al. Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch. Gen. Psychiatry 57, 1061-1069 (2000).
10. Huang, H. S. & Akbarian, S. GAD1 mRNA expression and DNA methylation in prefrontal cortex of subjects with schizophrenia. PloS One 2, e809 (2007).
11. Lewis, D. A., Curley, A. A., Glausier, J. R. & Volk, D. W. Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia. Trends Neurosci. 35, 57-67 (2012).
12. Mirnics, K., Middleton, F. A., Marquez, A., Lewis, D. A. & Levitt, P. Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex. Neuron 28, 53-67 (2000).
13. Thompson, M., Weickert, C. S., Wyatt, E. & Webster, M. J. Decreased glutamic acid decarboxylase(67) mRNA expression in multiple brain areas of patients with schizophrenia and mood disorders. J. Psychiatr. Res. 43, 970-977 (2009).
14. Beasley, C. L. & Reynolds, G. P. Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics. Schizophr. Res. 24, 349-355 (1997).
15. Hashimoto, T. et al. Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J. Neurosci. 23, 6315-6326 (2003).
16. Nestler, E. J. & Hyman, S. E. Animal models of neuropsychiatric disorders. Nat. Neurosci. 13, 1161-1169 (2010).
17. Fazzari, P. et al. Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling. Nature 464, 1376-1380 (2010).
18. Hikida, T. et al. Dominant-negative DISC1 transgenic mice display schizophrenia-associated phenotypes detected by measures translatable to humans. Proc. Natl. Acad. Sci. USA 104, 14501-14506 (2007).
19. Marin, O. Interneuron dysfunction in psychiatric disorders. Nat. Rev. Neurosci. 13, 107-120 (2012).
20. Shen, S. et al. Schizophrenia-related neural and behavioral phenotypes in transgenic mice expressing truncated Disc1. J. Neurosci. 28, 10893-10904 (2008).
21. Wen, L. et al. Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons. Proc. Natl. Acad. Sci. USA 107, 1211-1216 (2010).
22. Behrens, M. M. et al. Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science 318, 1645-1647 (2007).
23. Morris, B. J., Cochran, S. M. & Pratt, J. A. PCP: from pharmacology to modelling schizophrenia. Curr. Opin. Pharmacol. 5, 101-106 (2005).
24. Lisman, J. E. et al. Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci. 31, 234-242 (2008).
25. Markram, H. et al. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5, 793-807 (2004).
26. Murray, A. J. et al. Parvalbumin-positive CA1 interneurons are required for spatial working but not for reference memory. Nat. Neurosci. 14, 297-299 (2011).
27. Hippenmeyer, S. et al. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol. 3, e159 (2005).
28. Holmes, A. et al. Early life genetic, epigenetic and environmental factors shaping emotionality in rodents. Neurosci. Biobehav. Rev. 29, 1335-1346 (2005).
29. McAlonan, K. & Brown, V. J. Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behav. Brain Res. 146. 97-103 (2003).
30. Uylings, H. B., Groenewegen, H. J. & Kolb, B. Do rats have a prefrontal cortex? Behav. Brain Res. 146, 3-17 (2003).
31. Yamamoto M. Reversable suppression of glutamatergic neurotransmission of cerebellar granule cells in vivo by genetically manipulated expression of tetanus neurotoxin light chain. J. Neurosci. 23: 6759-6767 (2003).
32. Jarrard, L. E. On the use of ibotenic acid to lesion selectively different components of the hippocampal formation. J. Neurosci. Methods 29, 251-259 (1989).
33. Jaskiw, G. E. et al. Effect of ibotenic acid lesions of the medial prefrontal cortex on amphetamine-induced locomotion and regional brain catecholamine concentrations in the rat. Brain Res. 534, 263-272 (1990).
34. Deacon, R. M., Penny, C. & Rawlins, J. N. Effects of medial prefrontal cortex cytotoxic lesions in mice. Behav. Brain Res. 139, 139-155 (2003)
35. Fuster, J. M. The prefrontal cortex-an update: time is of the essence. Neuron 30, 319-333 (2001).
36. de Bruin, J. P. A behavioural analysis of rats with damage to the medial prefrontal cortex using the Morris water maze: evidence for behavioural flexibility, but not for impaired spatial navigation. Brain Res. 652, 323-333 (1994).
37. Lacroix, L., White, I. & Feldon, J. Effect of excitotoxic lesions of rat medial prefrontal cortex on spatial memory. Behav. Brain Res. 133, 69-81 (2002).
38. Barch, D. M. & Ceaser, A. Cognition in schizophrenia: core psychological and neural mechanisms. Trends Cogn. Sci. 16, 27-34 (2012).
39. Kellendonk, C., Simpson, E. H. & Kandel, E. R. Modeling cognitive endophenotypes of schizophrenia in mice. Trends Neurosci. 32, 347-358 (2009).
40. Kesner, R. P., Hunt, M. E., Williams, J. M. & Long, J. M. Prefrontal cortex and working memory for spatial response, spatial location, and visual object information in the rat. Cereb. Cortex. 6, 311-318 (1996).
41. Floresco, S. B., Seamans, J. K. & Phillips, A. G. Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without delay. J. Neurosci. 17, 1880-1890 (1997).
42. Eichenbaum, H., Clegg, R. A. & Feeley, A. Reexamination of functional subdivisions of the rodent prefrontal cortex. Exp. Neurol. 79, 434-451 (1983).
43. Leeson, V. C. et al. 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, 586-593 (2009).
44. Waltz, J. A. & Gold, J. M. Probabilistic reversal learning impairments in schizophrenia: further evidence of orbitofrontal dysfunction. Schizophr. Res. 93, 296-303 (2007).
45. Arguello, P. A. & Gogos, J. A. Modeling madness in mice: one piece at a time. Neuron 52, 179-196 (2006).
46. Forbes, C. E. & Grafman, J. The role of the human prefrontal cortex in social cognition and moral judgment. Annu. Rev. Neurosci. 33, 299-324 (2010).
47. Li, C. R., Huang, G. B., Sui, Z. Y., Han, E. H. & Chung, Y. C. Effects of 6-hydroxydopamine lesioning of the medial prefrontal cortex on social interactions in adolescent and adult rats. Brain Res. 1346, 183-189 (2010).
48. Rangel, A., Gonzalez, L. E., Villarroel, V. & Hernandez, L. Anxiolysis followed by anxiogenesis relates to coping and corticosterone after medial prefrontal cortical damage in rats. Brain Res. 992, 96-103 (2003).
49. Riedel, G., Kang, S. H., Choi, D. Y. & Platt, B. Scopolamine-induced deficits in social memory in mice: reversal by donepezil. Behav. Brain Res. 204, 217-225 (2009).
50. Laruelle, M., Abi-Dargham, A., Gil, R., Kegeles, L. & Innis, R. Increased dopamine transmission in schizophrenia: relationship to illness phases. Biol. Psychiatry 46, 56-72 (1999).
51. Lieberman, J. A., Kane, J. M. & Alvir, J. Provocative tests with psychostimulant drugs in schizophrenia. Psychopharmacology 91, 415-433 (1987).
52. Bertolino, A. et al. The relationship between dorsolateral prefrontal neuronal N-acetylaspartate and evoked release of striatal dopamine in schizophrenia. Neuropsychopharmacology 22, 125-132 (2000).
53. Sesack, S. R. & Carr, D. B. Selective prefrontal cortex inputs to dopamine cells: implications for schizophrenia. Physiol. Behav. 77, 513-517 (2002).
54. Baddeley, A. Working memory. Curr. Biol. CB 20, R136-140 (2010).
55. Goldman-Rakic, P. S. The physiological approach: functional architecture of working memory and disordered cognition in schizophrenia. Biol. Psychiatry 46, 650-661 (1999).
56. Howard, M. W. et al. Gamma oscillations correlate with working memory load in humans. Cereb. Cort. 13, 1369-1374 (2003).
57. Jones, M. W. & Wilson, M. A. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol. 3, e402 (2005).
58. Fuchs, E. C. et al. Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior. Neuron 53, 591-604 (2007).
59. Lodge, D. J., Behrens, M. M. & Grace, A. A. A loss of parvalbumin-containing interneurons is associated with diminished oscillatory activity in an animal model of schizophrenia. J. Neurosci. 29, 2344-2354 (2009).
60. Sohal, V. S., Zhang, F., Yizhar, O. & Deisseroth, K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459, 698-702 (2009).
61. Wulff, P. et al. Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbuminpositive interneurons. Proc. Natl. Acad. Sci. USA 106, 3561-3566 (2009).
62. Kehagia, A. A., Murray, G. K. & Robbins, T. W. Learning and cognitive flexibility: frontostriatal function and monoaminergic modulation. Curr. Opin. Neurobiol. 20, 199-204 (2010).
63. Hanslmayr, S. et al. Prefrontally driven downregulation of neural synchrony mediates goal-directed forgetting. J. Neurosci. 32, 14742-14751 (2012).
64. O'Tuathaigh, C. M., Kirby, B. P., Moran, P. M. & Waddington, J. L. Mutant mouse models: genotype-phenotype relationships to negative symptoms in schizophrenia. Schizophr. Bull. 36, 271-288 (2010).
65. Covington, H. E. et al. Antidepressant effect of optogenetic stimulation of the medial prefrontal cortex. J. Neurosci. 30, 16082-16090 (2010).
66. Celada, P., Puig, M. V., Casanovas, J. M., Guillazo, G. & Artigas, F. Control of dorsal raphe serotonergic neurons by the medial prefrontal cortex: Involvement of serotonin-1A, GABA(A), and glutamate receptors. J. Neurosci. 21, 9917-9929 (2001).
67. Chaudhury, D. et al. Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature 493, 532-536 (2013).
68. Enomoto, T., Tse, M. T. & Floresco, S. B. Reducing prefrontal gamma-aminobutyric acid activity induces cognitive, behavioral, and dopaminergic abnormalities that resemble schizophrenia. Biol. Psychiatry, 69, 432-441 (2011).
69. Auger, M. L. & Floresco, S. B. Prefrontal cortical GABA modulation of spatial reference and working memory. Int. J. Neuropsychopharmacol. 18, 1-11 (2014).
70. Hernan et al. Focal epileptiform activity in the prefrontal cortex is associated with long-term attention and sociability deficits. Neurobiol. Dis. 63, 25-34 (2014).
71. Taniguchi H. et al. A resource of cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71, 995-1013 (2011).
72. McClure, C., Cole, K. L., Wulff, P., Klugmann, M. & Murray, A. J. Production and titering of recombinant adeno-associated viral vectors. J. Vis. Exp. 57, e3348 (2011).
73. Paxinos, G. & Franklin, K. B. J. The mouse brain in stereotaxic coordintaes. Academic Press (2008).