Region-specific reduction in entorhinal gamma oscillations and parvalbumin-immunoreactive neurons in animal models of psychiatric illness

Journal of Neuroscience

Volumn 26, Issue 10, 2006, Pages 2767-2776

  Cunningham, Mark O ^a   Hunt, Jillian ^a   Middleton, Steven ^b   LeBeau, Fiona E N ^a   Gillies, Martin G ^a   Davies, Ceri H ^c   Maycox, Peter R ^c   Whittington, Miles A ^a   Racca, Claudia ^a,d  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c GLAXOSMITHKLINE   (United Kingdom)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Entorhinal cortex; Gamma oscillation; Inhibition; Ketamine; LPA1 receptor; Schizophrenia

Indexed keywords

4 AMINOBUTYRIC ACID; CALRETININ; GLUTAMATE RECEPTOR; KAINIC ACID; LYSOPHOSPHATIDIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PARVALBUMIN; RECEPTOR SUBTYPE;

ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; AUTOPSY; BRAIN REGION; BRAIN SLICE; CONTROLLED STUDY; ENTORHINAL CORTEX; GAMMA RHYTHM; GENE EXPRESSION; HIPPOCAMPUS; IMMUNOREACTIVITY; INTERNEURON; MALE; MENTAL DISEASE; MOUSE; NEUROCHEMISTRY; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PSYCHOMOTOR ACTIVITY; RAT; SCHIZOPHRENIA; SYNAPSE;

ANIMALS; DISEASE MODELS, ANIMAL; ENTORHINAL CORTEX; EVOKED POTENTIALS; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; IMMUNOHISTOCHEMISTRY; KAINIC ACID; KETAMINE; MALE; MENTAL DISORDERS; MICE; MICE, KNOCKOUT; NEURAL INHIBITION; NEURONS; OSCILLOMETRY; PARVALBUMINS; TNF RECEPTOR-ASSOCIATED FACTOR 3;

EID: 33644824721     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5054-05.2006     Document Type: Article

References (67)

1. Adams B, Moghaddam B (1998) Corticolimbic dopamine neurotransmission is temporally dissociated from the cognitive and locomotor effects of phencyclidine. J Neurosci 18:5545-5554.
2. Adler CM, Malhotra AK, Elman I, Goldberg T, Egan M, Pickar D, Breier A (1999) Comparison of ketamine-induced thought disorder in healthy volunteers and thought disorder in schizophrenia. Am J Psychiatry 156:1646-1649.
3. Akbarian S, Kim JJ, Potkin SG, Hagman JO, Tafazzoli A, Bunney Jr WE, Jones EG (1995) Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. Arch Gen Psychiatry 52:258-266.
4. Aoki F, Fetz EE, Shupe L, Lettich E, Ojemann GA (1999) Increased gamma-range activity in human sensorimotor cortex during performance of visuomotor tasks. Clin Neurophysiol 110:524-537.
5. Arnold SE (2000) Cellular and molecular neuropathology of the parahippocampal region in schizophrenia. Ann NY Acad Sci 911:275-292.
6. Bachus SE, Hyde TM, Herman MM, Egan MF, Klienman JE (1997) Abnormal cholecystokinin mRNA levels in entorhinal cortex of schizophrenics. J Psychiatr Res 31:233-256.
7. Bergmann I, Nitsch R, Frotscher M (1991) Area-specific morphological and neurochemical maturation of non-pyramidal neurons in the rat hippocampus as revealed by parvalbumin immunocytochemistry. Anat Embryol (Berl) 184:403-409.
8. Borgers C, Epstein S, Kopell NJ (2005) Background gamma rhythmicity and attention in cortical local circuits: a computational study. Proc Natl Acad Sci USA 102:7002-7007.
9. Braff DL, Grillon C, Geyer MA (1992) Sensorimotor gating and schizophrenia. Arch Gen Psychiatry 49:206-215.
10. Brody SA, Dulawa SC, Conquet F, Geyer MA (2004) Assessment of a prepulse inhibition deficit in a mutant mouse lacking mGluR5 receptors. Mol Psychiatry 9:35-41.
11. Charpak S, Pare D, Llinás R (1995) The entorhinal cortex entrains fast CA1 hippocampal oscillations in the anaesthetized guinea-pig: role of the monosynaptic component of the perforant path. Eur J Neurosci 7:1548-1557.
12. Chrobak JJ, Buzsáki G (1998) Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 18:388-398.
13. Cochran SM, Fujimura M, Morris BJ, Pratt JA (2002) Acute and delayed effects of phencyclidine upon mRNA levels of markers of glutamatergic and GABAergic neurotransmitter function in the rat brain. Synapse 46:206-214.
14. Cochran SM, Kennedy M, McKerchar CE, Steward LJ, Pratt JA, Morris BJ (2003) Induction of metabolic hypofunction and neurochemical deficits after chronic intermittent exposure to phencyclidine: differential modulation by antipsychotic drugs. Neuropsychopharmacology 28:265-275.
15. Cunningham MO, Davies CH, Buhl EH, Kopell N, Whittington MA (2003) Gamma oscillations induced by kainate receptor activation in the entorhinal cortex in vitro. J Neurosci 23:9761-9769.
16. de Bruin NM, Ellenbroek BA, Cools AR, Coenen AM, van Luijtelaar EL (1999) Differential effects on gating of auditory evoked potentials and prepulse inhibition in rats. Psychopharmacology (Berl) 142:9-17.
17. Dickson CT, Biella G, de Curtis M (2000) Evidence for spatial modules mediated by temporal synchronization of carbachol-induced gamma rhythm in medial entorhinal cortex. J Neurosci 20:7846-7854.
18. Du J, Zhang L, Weiser M, Rudy B, McBain CJ (1996) Developmental expression and functional characterization of the potassium channel subunit Kv3.1b in parvalbumin-containing interneurons of the rat hippocampus. J Neurosci 16:506-518.
19. Dugladze T, Lepsveridze E, Breustedt J, Kehrer C, Heinemann U, Gloveli T (2004) Effects of phencyclidines on signal transfer from the entorhinal cortex to the hippocampus in rats. Neurosci Lett 354:185-188.
20. Ellison G (1995) The N-methyl-D-aspartate antagonists phencyclidine, ketamine and dizocilpine as both behavioral and anatomical models of the dementias. Brain Res Brain Res Rev 20:250-267.
21. Elvevag B, Goldberg TE (2000) Cognitive impairment in schizophrenia is the core of the disorder. Crit Rev Neurobiol 14:1-21.
22. Engel AK, Konig P, Kreiter AK, Singer W (1991) Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex. Science 252:1177-1179.
23. Falkai P, Schneider-Axmann T, Honer WG (2000) Entorhinal cortex pre-alpha clusters in schizophrenia: quantitative evidence of a developmental abnormality. Biol Psychiatry 47:937-943.
24. Fell J, Klaver P, Lehnertz K, Grunwald T, Schaller C, Elger CE, Fernandez G (2001) Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat Neurosci 4:1259-1264.
25. Fisahn A, Pike FG, Buhl EH, Paulsen O (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394:186-189.
26. Geyer MA, Braff DL (1987) Startle habituation and sensorimotor gating in schizophrenia and related animal models. Schizophr Bull 13:643-668.
27. Gloveli T, Dugladze T, Saha S, Monyer H, Heinemann U, Traub RD, Whittington MA, Buhl EH (2005) Differential involvement of oriens/pyramidale interneurons in hippocampal network oscillations in vitro. J Physiol (Lond) 562:131-147.
28. Gogos JA, Santha M, Takacs Z, Beck KD, Luine V, Lucas LR, Nadler JV, Karayiorgou M (1999) The gene encoding praline dehydrogenase modulates sensorimotor gating in mice. Nat Genet 21:434-439.
29. Goto K, Ueki A, Iso H, Morita Y (2002) Reduced prepulse inhibition in rats with entorhinal cortex lesions. Behav Brain Res 134:201-207.
30. Grunze HC, Rainnie DG, Hasselmo ME, Barkai E, Hearn EF, McCarley RW, Greene RW (1996) NMDA-dependent modulation of CA1 local circuit inhibition. J Neurosci 16:2034-2043.
31. Gulyas AI, Toth K, Danos P, Freund TF (1991) Subpopulations of GABAergic neurons containing parvalbumin, calbindin D28k, and cholecystokinin in the rat hippocampus. J Comp Neurol 312:371-378.
32. Harrison SM, Reavill C, Brown G, Brown JT, Cluderay JE, Crook B, Davies CH, Dawson LA, Grau E, Heidbreder C, Hemmati P, Hervieu G, Howarth A, Hughes ZA, Hunter AJ, Latcham J, Pickering S, Pugh P, Rogers DC, Shillam CS, Maycox PR (2003) LPA1 receptor-deficient mice have phenotypic changes observed in psychiatric disease. Mol Cell Neurosci 24:1170-1179.
33. Hashimoto T, Volk DW, Eggan SM, Mirnics K, Pierri JN, Sun Z, Sampson AR, Lewis DA (2003) Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J Neurosci 23:6315-6326.
34. Hemby SE, Gisberg SD, Brunk B, Arnold SE, Tojanowski JQ, Eberwine JH (2002) Gene expression profile for schizophrenia: discrete neuron transcription patterns in the entorhinal cortex. Arch Gen Psychiatry 59:631-640.
35. Jones RS, Buhl EH (1993) Basket-like interneurons in layer II of the entorhinal cortex exhibit a powerful NMDA-mediated synaptic excitation. Neurosci Lett 149:35-39.
36. Keilhoff G, Becker A, Grecksch G, Wolf G, Bernstein HG (2004) Repeated application of ketamine to rats induces changes in the hippocampal expression of parvalbumin, neuronal nitric oxide synthase and cFOS similar to those seen in human schizophrenia. Neuroscience 126:591-598.
37. Kingsbury MA, Rehen SK, Contos JJ, Higgins CM, Chun J (2003) Non-proliferative effects of lysophosphatidic acid enhance cortical growth and folding. Nat Neurosci 6:1292-1299.
38. Knable MB, Barci BM, Webster MJ, Meador-Woodruff J, Torrey EF (2004) Molecular abnormalities of the hippocampus in severe psychiatric illness: postmortem findings from the Stanley Neuropathology Consortium. Mol Psychiatry 9:609-620.
39. Lewis DA, Hashimoto T, Volk DW (2005) Cortical inhibitory interneurons and schizophrenia. Nat Rev Neurosci 6:312-324.
40. Mann EO, Suckling JM, Hajos N, Greenfield SA, Paulsen O (2005) Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro. Neuron 45:105-117.
41. Marshall L, Molle M, Bartsch P (1996) Event-related gamma band activity during passive and active oddball tasks. NeuroReport 7:1517-1520.
42. Meincke U, Light GA, Geyer MA, Braff DL, Gouzoulis-Mayfrank E (2004) Sensitization and habituation of acoustic startle reflex in patients with schizophrenia. Psychiatry Res 126:51-61.
43. Miltner WH, Braun C, Arnold M, Witte H, Taub E (1999) Coherence of gamma-band EEG activity as a basis for associative learning. Nature 397:391-393.
44. Nyiri G, Stephenson FA, Freund TF, Somogyi P (2003) Large variability in synaptic N-methyl-D-aspartate receptor density on interneurons and a comparison with pyramidal cell spines in the rat hippocampus. Neuroscience 119:347-363.
45. Oranje B, Gispen-de Wied CC, Verbaten MN, Kahn RS (2002) Modulating sensory gating in healthy volunteers: the effects of ketamine and haloperidol. Biol Psychiatry 52:887-895.
46. Park S, Holzman PS (1992) Schizophrenics show spatial working memory deficits. Arch Gen Psychiatry 49:975-982.
47. Prasad KM, Patel AR, Muddasani S, Sweeney J, Keshavan MS (2004) The entorhinal cortex in first-episode psychotic disorders: a structural magnetic resonance imaging study. Am J Psychiatry 161:1612-1619.
48. Roberts C, Winter P, Hughes ZA, Langmead C, Maycox PR, Dawson LA (2005) Neurochemical changes in LPA1 receptor-deficient mice - a putative model of schizophrenia. Neurochem Res 30:371-377.
49. Rodriguez E, George N, Lachaux JP, Martinerie J, Renault B, Varela FJ (1999) Perception's shadow: long-distance synchronisation of human brain activity. Nature 397:430-433.
50. Seeman P, Ko F, Tallerico T (2005) Dopamine receptor contribution to the action of PCP, LSD, and ketamine psychotomimetics. Mol Psychiatry 10:877-883.
51. Singer W, Gray CM (1995) Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18:555-586.
52. Solger J, Wozny C, Manahan-Vaughan D, Behr J (2004) Distinct mechanisms of bidirectional activity-dependent synaptic plasticity in superficial and deep layers of rat entorhinal cortex. Eur J Neurosci 19:2003-2007.
53. Spencer KM, Nestor PG, Niznikiewicz MA, Salisbury DF, Shenton ME, McCarley RW (2003) Abnormal neural synchrony in schizophrenia. J Neurosci 23:7407-7411.
54. Spencer KM, Nestor PG, Perlmutter R, Niznikiewicz MA, Klump MC, Frumin M, Shenton ME, McCarley RW (2004) Neural synchrony indexes disordered perception and cognition in schizophrenia. Proc Natl Acad Sci USA 101:17288-17293.
55. Tiitinen H, Sinkkonen J, Reinikainen K, Alho K, Lavikainen J, Naatanen R (1993) Selective attention enhances the auditory 40 Hz transient response in humans. Nature 364:59-60.
56. Tueting P, Costa E, Dwivedi Y, Guidotti A, Impagnatiello F, Manev R, Pesold C (1999) The phenotypic characteristics of heterozygous reeler mouse. NeuroReport 10:1329-1334.
57. Vaisanen J, Ihalainen J, Tanila H, Castren E (2004) Effects of NMDA receptor antagonist treatment on c-fos expression in rat brain areas implicated in schizophrenia. Cell Mol Neurobiol 24:769-780.
58. Weinberger DR (1997) The biological basis of schizophrenia: new directions. J Clin Psychiatry 58:22-27.
59. Weinberger DR, Berman KF, Zec RF (1986) Physiologic dysfunction of dorsolateral prefrontal cortex in schizophrenia. I. Regional cerebral blood flow evidence. Arch Gen Psychiatry 43:114-124.
60. A1/edg-2 is expressed by mature oligodendrocytes during myelination in the postnatal murine brain. J Comp Neurol 398:587-598.
61. Whittington MA, Traub RD (2003) Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci 26:676-682.
62. Whittington MA, Traub RD, Jefferys JG (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612-615.
63. Woo T-U, Whitehead RE, Melchitzky DS, Lewis DA (1998) A subclass of gamma aminobutyric acid axon terminals are selectively altered in schizophrenia. Proc Natl Acad Sci USA 95:5341-5346.
64. Woodhall GL, Bailey SJ, Thompson SE, Evans DI, Jones RS (2005) Fundamental differences in spontaneous synaptic inhibition between deep and superficial layers of the rat entorhinal cortex. Hippocampus 15:232-245.
65. Ylinen A, Bragin A, Nadasdy Z, Jando G, Szabo I, Sik A, Buzsáki G (1995) Sharp wave-associated high frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15:30-46.
66. Volk D, Austin M, Pierri J, Sampson A, Lewis D (2001) GABA transporter-1 mRNA in the prefrontal cortex in schizophrenia: decreased expression in a subset of neurons. Am J Psychiatry 158:256-265.
67. Zhang ZJ, Reynolds GP (2002) A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia. Schizophr Res 55:1-10.