A sensitive period for GABAergic interneurons in the dentate gyrus in modulating sensorimotor gating

Journal of Neuroscience

Volumn 33, Issue 15, 2013, Pages 6691-6704

  Guo, Nannan ^a,d   Yoshizaki, Kaichi ^a   Kimura, Ryuichi ^a   Suto, Fumikazu ^a,b   Yanagawa, Yuchio ^c   Osumi, Noriko ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^c GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; BROXURIDINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CELL STRUCTURE; CONTROLLED STUDY; DENDRITIC CELL; DENTATE GYRUS; EXPOSURE; FLUORESCENCE MICROSCOPY; FORCED SWIMMING TEST; HIPPOCAMPUS; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; INTERNEURON; MALE; MAZE TEST; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PREPULSE INHIBITION; PRIORITY JOURNAL; SENSORY GATING;

AGE FACTORS; ANIMALS; BEHAVIOR, ANIMAL; CRITICAL PERIOD (PSYCHOLOGY); DENDRITES; DENTATE GYRUS; DISEASE MODELS, ANIMAL; DRUG INTERACTIONS; ENVIRONMENT; GABA AGONISTS; GABAERGIC NEURONS; INHIBITION (PSYCHOLOGY); INTERNEURONS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; METHYLAZOXYMETHANOL ACETATE; MICE; MICE, INBRED C57BL; MICROINJECTIONS; MICROTUBULE-ASSOCIATED PROTEINS; MUSCIMOL; NEUROGENESIS; NEUROPEPTIDES; PREFRONTAL CORTEX; PROTEIN-SERINE-THREONINE KINASES; SCHIZOPHRENIA; SENSORY GATING;

EID: 84876004372     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0032-12.2013     Document Type: Article

References (62)

1. Bast T, Feldon J (2003) Hippocampal modulation of sensorimotor processes. Prog Neurobiol 70:319-345.
2. Bednarczyk MR, Hacker LC, Fortin-Nunez S, Aumont A, Bergeron R, Fer-nandes KJ (2011) Distinct stages of adult hippocampal neurogenesis are regulated by running and the running environment. Hippocampus 21: 1334-1347.
3. Braff DL, Light GA (2005) The use of neurophysiological endophenotypes to understand the genetic basis of schizophrenia. Dialogues Clin Neurosci 7:125-135.
4. Braff DL, Geyer MA, Swerdlow NR (2001) Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl) 156:234-258.
5. Brenes JC, Rodríguez O, Fornaguera J (2008) Differential effect of environment enrichment and social isolation on depressive-like behavior, spontaneous activity and serotonin and norepinephrine concentration in prefrontal cortex and ventral striatum. Pharmacol Biochem Behav 89:85-93.
6. Cadenhead KS, Light GA, Geyer MA, Braff DL (2000) Sensory gating deficits assessed by the P50 event-related potential in subjects with schizo-typal personality disorder. Am J Psychiatry 157:55-59.
7. Cattaneo E, Reinach B, Caputi A, Cattabeni F, Di Luca M (1995) Selective in vitro blockade of neuroepithelial cells proliferation by methylazoxy-methanol, a molecule capable of inducing long lasting functional impairments. J Neurosci Res 41:640-647.
8. Charych EI, Liu F, Moss SJ, Brandon NJ (2009) GABA(A) receptors and their associated proteins: implications in the etiology and treatment of schizophrenia and related disorders. Neuropharmacology 57:481-495.
9. Cherlyn SY, Woon PS, Liu JJ, Ong WY, Tsai GC, Sim K (2010) Genetic association studies of glutamate, GABA and related genes in schizophrenia and bipolar disorder: a decade of advance. Neurosci Biobehav Rev 34:958-977.
10. Ciaroni S, Cuppini R, Cecchini T, Ferri P, Ambrogini P, Cuppini C, Del Grande P (1999) Neurogenesisin the adult rat dentate gyrusis enhanced by vitamin E deficiency. J Comp Neurol 411:495-502.
11. Ciaroni S, Cecchini T, Ferri P, Ambrogini P, Cuppini R, Lombardelli G, Peruzzi G, Del Grande P (2002) Postnatal development of rat dentate gyrus: effects of methylazoxymethanol administration. Mech Ageing Dev 123:499-509.
12. Doischer D, Hosp JA, Yanagawa Y, Obata K, Jonas P, Vida I, Bartos M (2008) Postnatal differentiation of basket cells from slow to fast signaling devices. J Neurosci 28:12956-12968.
13. Douaud G, Mackay C, Andersson J, James S, Quested D, Ray MK, Connell J, Roberts N, Crow TJ, Matthews PM, Smith S, James A (2009) Schizophrenia delays and alters maturation of the brain in adolescence. Brain 132:2437-2448.
14. Eisch AJ, Cameron HA, Encinas JM, Meltzer LA, Ming GL, Overstreet-Wadiche LS (2008) Adult neurogenesis, mental health, and mental illness: hope or hype? J Neurosci 28:11785-11791.
15. Flagstad P, Mørk A, Glenthøj BY, van Beek J, Michael-Titus AT, Didriksen M (2004) Disruption of neurogenesis on gestational day 17 in the rat causes behavioral changes relevant to positive and negative schizophrenia symptoms and alters amphetamine-induced dopamine release in nucleus ac-cumbens. Neuropsychopharmacology 29:2052-2064.
16. Fleming RL, Wilson WA, Swartzwelder HS (2007) Magnitude and ethanol sensitivity of tonic GABAA receptor-mediated inhibition in dentate gyrus changes from adolescence to adulthood. J Neurophysiol 97:3806-3811.
17. Gogtay N, Vyas NS, Testa R, Wood SJ, Pantelis C (2011) Age of onset of schizophrenia: perspectives from structural neuroimaging studies. Schizophr Bull 37:504-513.
18. Guidotti A, Auta J, Davis JM, Dong E, Grayson DR, Veldic M, Zhang X, Costa E (2005) GABAergic dysfunction in schizophrenia: new treatment strategies on the horizon. Psychopharmacology (Berl) 180:191-205.
19. Haddad RK, Rabe A, Dumas R (1972) Comparison of effects of methyla-zoxymethanol acetate on brain development indifferent species. Fed Proc 31:1520-1523.
20. Harte MK, Powell SB, Swerdlow NR, Geyer MA, Reynolds GP (2007) Deficitsin parvalbumin and calbindin immunoreactive cells in the hippocampus of isolation reared rats. J Neural Transm 114:893-898.
21. Hayashi F, Takashima N, Murayama A, Inokuchi K (2008) Decreased postnatal neurogenesis in the hippocampus combined with stress experience during adolescence is accompanied by an enhanced incidence of behavioral pathologies in adult mice. Mol Brain 1:22.
22. He J, Crews FT (2007) Neurogenesis decreases during brain maturation from adolescence to adulthood. Pharmacol Biochem Behav 86:327-333.
23. Heckers S, Konradi C (2010) Hippocampal pathology in schizophrenia. Curr Top Behav Neurosci 4:529-553.
24. Hoskison MM, Yanagawa Y, Obata K, Shuttleworth CW (2007) Calcium-dependent NMDA-induced dendric injury and MAP2 loss in acute hip-pocampal slices. Neuroscience 145:66-79.
25. Hyde TM, Lipska BK, Ali T, Mathew SV, Law AJ, Metitiri OE, Straub RE, Ye T, Colantuoni C, Herman MM, Bigelow LB, Weinberger DR, Kleinman JE (2011) Expression of GABA signaling molecules KCC2, NKCC1, and GAD1 in cortical development and schizophrenia. J Neurosci 31:11088-11095.
26. Kapur J, Macdonald RL (1999) Postnatal development of hippocampal dentate granule cell gamma-aminobutyric acidA receptor pharmacological properties. Mol Pharmacol 55:444-452.
27. Kempermann G, Kuhn HG, Gage FH (1997) More hippocampalneurons in adult mice living in an enriched environment. Nature 386:493-495.
28. Kempermann G, Gast D, Gage FH (2002) Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann Neurol 52:135-143.
29. Kempermann G, Krebs J, Fabel K (2008) The contribution of failing adult hippocampal neurogenesis to psychiatric disorders. Curr Opin Psychiatry 21:290-295.
30. Lewis DA (1997) Development of the prefrontal cortex during adolescence: insights into vulnerable neural circuits in schizophrenia. Neu-ropsychopharmacology 16:385-398.
31. Lewis DA, Levitt P (2002) Schizophrenia as a disorder of neurodevelopment. Annu RevNeurosci 25:409-432.
32. Lewis DA, Cruz D, Eggan S, Erickson S (2004) Postnatal development of prefrontal inhibitory circuits and the pathophysiology of cognitive dysfunction in schizophrenia. Ann NY Acad Sci 1021:64-76.
33. Lodge DJ, Behrens MM, Grace AA (2009) Alossofparvalbumin-containing interneurons is associated with diminished oscillatory activity in an animal model of schizophrenia. J Neurosci 29:2344-2354.
34. Louchart- de la Chapelle S, Nkam I, Houy E, Belmont A, Menard JF, Rous-signol AC, Siwek O, Mezerai M, Guillermou M, Fouldrin G, Levillain D, Dollfus S, Campion D, Thibaut F (2005) A concordance study of three electrophysiological measures in schizophrenia. Am J Psychiatry 162: 466-474.
35. Maekawa M, Takashima N, Matsumata M, Ikegami S, Kontani M, Hara Y, Kawashima H, Owada Y, Kiso Y, Yoshikawa T, Inokuchi K, Osumi N (2009) Arachidonic acid drives postnatal neurogenesis and elicits a beneficial effect on prepulse inhibition, a biological trait of psychiatric illnesses. PLoS One 4:e5085.
36. Manning EE, Ransome MI, Burrows EL, Hannan AJ (2012) Increased adult hippocampal neurogenesis and abnormal migration of adult-born granule neurons is associated with hippocampal-specific cognitive deficits in phospholipase C-/31 knockout mice. Hippocampus 22:309-319.
37. Matsumata M, Sakayori N, Maekawa M, Owada Y, Yoshikawa T, Osumi N (2012) The effects of Fabp7 and Fabp5 on postnatal hippocampal neurogenesis in the mouse. Stem Cells 30:1532-1543.
38. McOmish CE, Burrows E, Howard M, Scarr E, Kim D, Shin HS, Dean B, van den Buuse M, Hannan AJ (2008) Phospholipase C-beta1 knockout mice exhibit endophenotypes modeling schizophrenia which are rescued by environmental enrichment and clozapine administration. Mol Psychiatry 13:661-672.
39. Meshi D, Drew MR, Saxe M, Ansorge MS, David D, Santarelli L, Malapani C, Moore H, Hen R (2006) Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nat Neurosci 9:729-731.
40. Nithianantharajah J, Hannan AJ (2006) Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7:697-709.
41. Osumi N, Guo N (2011) Impaired neuroscience as a risk factor for schizophrenia and related mental diseases. In: Neurogenesis in the Adult Brain II (Seki T, Sawamoto K, Parent JM, Alvarez-Buylla A, eds), pp 109-131. Tokyo: Springer.
42. Penschuck S, Flagstad P, Didriksen M, Leist M, Michael-Titus AT (2006) Decrease in parvalbumin-expressing neurons in the hippocampus and increased phencyclidine-induced locomotor activity in the rat methy-lazoxymethanol (MAM) model of schizophrenia. Eur J Neurosci 23: 279-284.
43. Pieper AA, Xie S, Capota E, Estill SJ, Zhong J, Long JM, Becker GL, Huntington P, Goldman SE, Shen CH, Capota M, Britt JK, Kotti T, Ure K, Brat DJ, Williams NS, MacMillan KS, Naidoo J, Melito L, Hsieh J et al. (2010) Discovery of a proneurogenic, neuroprotective chemical. Cell 142:39-51.
44. Plümpe T, Ehninger D, Steiner B, Klempin F, Jessberger S, Brandt M, Romer B, Rodriguez GR, Kronenberg G, Kempermann G (2006) Variability of double cortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci 7:77.
45. Rapoport JL, Addington AM, Frangou S, Psych MR (2005) The neuro developmental model of schizophrenia: update 2005. Mol Psychiatry 10:434-449.
46. Redolat R, Mesa-Gresa P (2012) Potential benefits and limitations of enriched environments and cognitive activity on age-related behavioral decline. Curr Top Behav Neurosci 10:293-316.
47. Rudolph U, Knoflach F (2011) Beyond classical benzodiazepines: novel therapeutic potential of GABAA receptor subtypes. Nat Rev Drug Discov 10:685-697.
48. Saint Marie RL, Miller EJ, Breier MR, Weber M, Swerdlow NR (2010) Projections from ventral hippocampus to medial prefrontal cortex but not nucleus accumbens remain functional after for nix lesions in rats. Neuro-science 168:498-504.
49. Schloesser RJ, Lehmann M, Martinowich K, Manji HK, Herkenham M (2010)Environmental enrichment requires adult neurogenesis to facilitate the recovery from psychosocial stress. Mol Psychiatry 15:1152-1163.
50. Silva CF, Duarte FS, Lima TC, de Oliveira CL (2011) Effects of social isolation and enriched environment on behavior of adult Swiss mice do not require hippocampal neurogenesis. Behav Brain Res 225:85-90.
51. Sisk CL, Zehr JL (2005) Pubertal hormones organize the adolescent brain and behavior. Front Neuroendocrinol 26:163-174.
52. Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417-463.
53. Sun Y, Farzan F, Barr MS, Kirihara K, Fitzgerald PB, Light GA, Daskalakis ZJ (2011)Gamma oscillations in schizophrenia: mechanisms and clinical significance. Brain Res 1413:98-114.
54. Swerdlow NR, Geyer MA (1998) Using an animal model of deficient senso-rimotor gating to study the pathophysiology and new treatments of schizophrenia. Schizophr Bull 24:285-301.
55. Swerdlow NR, Weber M, Qu Y, Light GA, Braff DL (2008) Realistic expectations of prepulse inhibition in translational models for schizophrenia research. Psychopharmacology (Berl) 199:331-388.
56. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T (2003) Green fluorescent protein expression and colocalization with cal-retinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467:60-79.
57. Tamminga CA, Stan AD, Wagner AD (2010) The hippocampal formation in schizophrenia. Am J Psychiatry 167:1178-1193.
58. Thomas RM, Peterson DA (2008) Even neural stem cells get the blues: evidence for a molecular link between modulation of adult neurogenesis and depression. Gene Expr 14:183-193.
59. Tseng KY, Lewis BL, Hashimoto T, Sesack SR, Kloc M, Lewis DA, O'Donnell P (2008) A neonatal ventral hippocampal lesion causes functional deficits in adult prefrontal cortical interneurons. J Neurosci 28:12691-12699.
60. Vinkers CH, Mirza NR, Olivier B, Kahn RS (2010) The inhibitory GABA system as a therapeutic target for cognitive symptoms in schizophrenia: investigational agents in the pipeline. Expert Opin Investig Drugs 19: 1217-1233.
61. Volz A, Khorsand V, Gillies D, Leucht S (2007) Benzodiazepines for schizophrenia. Cochrane Database Syst Rev 1:CD006391.
62. Weinberger DR (1996) On the plausibility of "the neurodevelopmental hypothesis" of schizophrenia. Neuropsychopharmacology 14:1S-11S.