Differential Alterations of Auditory Gamma Oscillatory Responses between Pre-Onset High-Risk Individuals and First-Episode Schizophrenia

Cerebral Cortex

Volumn 26, Issue 3, 2016, Pages 1027-1035

  Tada, Mariko ^a   Nagai, Tatsuya ^a   Kirihara, Kenji ^a   Koike, Shinsuke ^a,b   Suga, Motomu ^a   Araki, Tsuyoshi ^a   Kobayashi, Tetsuo ^c   Kasai, Kiyoto ^a,d  

^a UNIVERSITY OF TOKYO   (Japan)

^b Office for Mental Health Support   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Auditory steady state response; electroencephalogram; gamma oscillations; schizophrenia; ultra high risk

Indexed keywords

BENZODIAZEPINE; BIOLOGICAL MARKER; NEUROLEPTIC AGENT;

ADOLESCENT; ADULT; ARTICLE; ATTENTION; AUDITORY RESPONSE; AUDITORY STEADY STATE RESPONSE; BRAIN FUNCTION; CLINICAL ARTICLE; COGNITION; CONTROLLED STUDY; EARLY DIAGNOSIS; ELECTROENCEPHALOGRAM; FEMALE; HIGH RISK POPULATION; HUMAN; MALE; PRIORITY JOURNAL; SCHIZOPHRENIA; ACUTE DISEASE; AUDITORY EVOKED POTENTIAL; AUDITORY STIMULATION; ELECTROENCEPHALOGRAPHY; GAMMA RHYTHM; HEARING; PATHOPHYSIOLOGY; PHYSIOLOGY; PRODROMAL SYMPTOM; PSYCHOLOGICAL INTERVIEW; PSYCHOLOGICAL RATING SCALE; PSYCHOTIC DISORDERS; RISK; YOUNG ADULT;

ACOUSTIC STIMULATION; ACUTE DISEASE; ANTIPSYCHOTIC AGENTS; ATTENTION; AUDITORY PERCEPTION; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, AUDITORY; FEMALE; GAMMA RHYTHM; HUMANS; INTERVIEW, PSYCHOLOGICAL; MALE; PRODROMAL SYMPTOMS; PSYCHIATRIC STATUS RATING SCALES; PSYCHOTIC DISORDERS; RISK; SCHIZOPHRENIA; YOUNG ADULT;

EID: 84961262969     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhu278     Document Type: Article

References (55)

1. Amann LC, Gandal MJ, Halene TB, Ehrlichman RS, White SL, McCarren HS, Siegel SJ. 2010. Mouse behavioral endophenotypes for schizophrenia. Brain Res Bull. 83:147-161.
2. American Psychiatric Association. 1994. Diagnostic and statistical manual ofmental disorders, 4th ed.Washington, DC:American Psychiatric Press.
3. Andreasen NC, Nopoulos P, Magnotta V, Pierson R, Ziebell S, Ho BC. 2011. Progressive brain change in schizophrenia:A prospective longitudinal study of first-episode schizophrenia. Biol Psychiatry. 70:672-679.
4. Brenner CA, Krishnan GP, Vohs JL, Ahn WY, Hetrick WP, Morzorati SL, O'Donnell BF. 2009. Steady state responses: electrophysiological assessment of sensory function in schizophrenia. Schizophr Bull. 35:1065-1077.
5. Brenner CA, Sporns O, Lysaker PH, O'Donnell BF. 2003. EEG synchronization to modulated auditory tones in schizophrenia, schizoaffective disorder, and schizotypal personality disorder. Am J Psychiatry. 160:2238-2240.
6. Cannon TD, Cadenhead K, Cornblatt B, Woods SW, Addington J, Walker E, Seidman LJ, Perkins D, Tsuang M, McGlashan T, et al. 2008. Prediction of psychosis in youth at high clinical risk: a multisite longitudinal study in North America. Arch Gen Psychiatry. 65:28-37.
7. Cardin JA, Carlen M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI. 2009. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature. 459:663-667.
8. Cho RY, Walker CP, Polizzotto NR, Wozny TA, Fissell A, Chen A, Lewis DA. 2015. Development of sensory gamma oscillations and cross-frequency coupling from childhood to early adulthood. Cereb Cortex. 25:1509-1518.
9. Delorme A, Makeig S. 2004. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods. 134:9-21.
10. Fisahn A, Neddens J, Yan L, Buonanno A. 2009. Neuregulin-1 modulates hippocampal gamma oscillations: implications for schizophrenia. Cereb Cortex. 19:612-618.
11. Fries P. 2009. Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci. 32:209-224.
12. Galambos R, Makeig S, Tarmachoff PJ. 1981. A 40-Hz auditory potential recorded from the human scalp. Proc Natl Acad Sci USA. 78:2643-2647.
13. Gonzalez-Burgos G, Lewis DA. 2008. GABA neurons and the mechanisms of network oscillations: implications for understanding cortical dysfunction in schizophrenia. Schizophr Bull. 34:944-961.
14. Hashimoto T, Arion D, Unger T, Maldonado-Aviles JG, Morris HM, Volk DW, Mimics K, Lewis DA. 2008. Alterations in GABArelated transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol Psychiatry. 13:147-161.
15. Hashimoto T, Nguyen QL, Rotaru D, Keenan T, Arion D, Beneyto M, Gonzalez-Burgos G, Lewis DA. 2009. Protracted developmental trajectories of GABAA receptor alpha1 and alpha2 subunit expression in primate prefrontal cortex. Biol Psychiatry. 65:1015-1023.
16. Hoftman GD, Lewis DA. 2011. Postnatal developmental trajectories of neural circuits in the primate prefrontal cortex: identifying sensitive periods for vulnerability to schizophrenia. Schizophr Bull. 37:493-503.
17. Hong LE, Summerfelt A, McMahon R, Adami H, Francis G, Elliott A, Buchanan RW, Thaker GK. 2004. Evoked gamma band synchronization and the liability for schizophrenia. Schizophr Res. 70:293-302.
18. Iwashiro N, Suga M, Takano Y, Inoue H, Natsubori T, Satomura Y, Koike S, Yahata N, Murakami M, Katsura M, et al. 2012. Localized gray matter volume reductions in the pars triangularis of the inferior frontal gyrus in individuals at clinical high-risk for psychosis and first episode for schizophrenia. Schizophr Res. 137:124-131.
19. Jahshan C, Cadenhead KS, Rissling AJ, Kirihara K, Braff DL, Light GA. 2012. Automatic sensory information processing abnormalities across the illness course of schizophrenia. Psychol Med. 42:85-97.
20. Kaneda Y, Sumiyoshi T, Keefe R, Ishimoto Y, Numata S, Ohmori T. 2007. Brief assessment of cognition in schizophrenia: validation of the Japanese version. Psychiatry Clin Neurosci. 61:602-609.
21. Kasai K. 2013. Toward an interdisciplinary science of adolescence: insights from schizophrenia research. Neurosci Res. 75:89-93.
22. Kasai K, Shenton ME, Salisbury DF, Hirayasu Y, Onitsuka T, Spencer KM, Yurgelun-Todd DA, Kikinis R, Jolesz FA, McCarley RW. 2003. Progressive decrease of left Heschl gyrus and planum temporale gray matter volume in first-episode schizophrenia: a longitudinal magnetic resonance imaging study. Arch Gen Psychiatry. 60:766-775.
23. Kay SR, Fiszbein A, Opler LA. 1987. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull. 13:261-276.
24. Keefe RS, Goldberg TE, Harvey PD, Gold JM, Poe MP, Coughenour L. 2004. The Brief Assessment of Cognition in Schizophrenia: reliability, sensitivity, and comparison with a standard neurocognitive battery. Schizophr Res. 68:283-297.
25. Keefe RS, Poe M, Walker TM, Harvey PD. 2006. The relationship of the Brief Assessment of Cognition in Schizophrenia (BACS) to functional capacity and real-world functional outcome. J Clin Exp Neuropsychol. 28:260-269.
26. Kirihara K, Rissling AJ, Swerdlow NR, Braff DL, Light GA. 2012. Hierarchical organization of gamma and theta oscillatory dynamics in schizophrenia. Biol Psychiatry. 71:873-880.
27. Kobayashi H, Nozaki S, Mizuno M. 2007. Reliability of the Structured Interview for Prodromal Syndromes Japanese version (SIPS-J). Jpn Bull Soc Psychiatry. 15:168-174.
28. Koike S, Takano Y, Iwashiro N, Satomura Y, Suga M, Nagai T, Natsubori T, Tada M, Nishimura Y, Yamasaki S, et al. 2013. A multimodal approach to investigate biomarkers for psychosis in a clinical setting: the integrative neuroimaging studies in schizophrenia targeting for early intervention and prevention (IN-STEP) project. Schizophr Res. 143:116-124.
29. Koike S, Takizawa R, Nishimura Y, Takano Y, Takayanagi Y, Kinou M, Araki T, Harima H, Fukuda M, Okazaki Y, et al. 2011. Different hemodynamic response patterns in the prefrontal cortical sub-regions according to the clinical stages of psychosis. Schizophr Res. 132:54-61.
30. Kwon JS, O'Donnell BF, Wallenstein GV, Greene RW, Hirayasu Y, Nestor PG, Hasselmo ME, Potts GF, Shenton M, McCarley RW. 1999.Gamma frequency-range abnormalities to auditory stimulation in schizophrenia. Arch Gen Psychiatry. 56:1001-1005.
31. Light GA, Hsu JL, Hsieh MH, Meyer-Gomes K, Sprock J, Swerdlow NR, Braff DL. 2006. Gamma band oscillations reveal neural network cortical coherence dysfunction in schizophrenia patients. Biol Psychiatry. 60:1231-1240.
32. Marshall M, Lewis S, Lockwood A, Drake R, Jones P, Croudace T. 2005. Association between duration of untreated psychosis and outcome in cohorts of first-episode patients: a systematic review. Arch Gen Psychiatry. 62:975-983.
33. Matsuoka K, Uno M, Kasai K, Koyama K, Kim Y. 2006. Estimation of premorbid IQ in individuals with Alzheimer's disease using Japanese ideographic script (Kanji) compound words: Japanese version of National Adult Reading Test. Psychiatry Clin Neurosci. 60:332-339.
34. Miller TJ, McGlashan TH, Woods SW, Stein K, Driesen N, Corcoran CM, Hoffman RH, Davidson L. 1999. Symptom assessment in schizophrenic prodromal states. Psychiatr Q. 70:273-287.
35. Minzenberg MJ, Firl AJ, Yoon JH, Gomes GC, Reinking C, Carter C. 2010. Gamma oscillatory power is impaired during cognitive control independent of medication status in first-episode schizophrenia. Neuropsychopharmacology. 35:2590-2599.
36. Moyer CE, Delevich KM, Fish KN, Asafu-Adjei JK, Sampson AR, Dorph-Petersen KA, Lewis DA, Sweet RA. 2012. Reduced glutamate decarboxylase 65 protein within primary auditory cortex inhibitory boutons in schizophrenia. Biol Psychiatry. 72:734-743.
37. O'Donnell BF, Hetrick WP, Vohs JL, Krishnan GP, Carroll CA, Shekhar A. 2004. Neural synchronization deficits to auditory stimulation in bipolar disorder. Neuroreport. 15:1369-1372.
38. Rojas DC, Maharajh K, Teale PD, Kleman MR, Benkers TL, Carlson JP, Reite ML. 2006. Development of the 40 Hz steady state auditory evoked magnetic field from ages 5 to 52. Clin Neurophysiol. 117:110-117.
39. Ross B, Picton TW, Pantev C. 2002. Temporal integration in the human auditory cortex as represented by the development of the steady-state magnetic field. Hear Res. 165:68-84.
40. Ruhrmann S, Schultze-Lutter F, Salokangas RKR, Heinimaa M, Linszen D, Dingemans P, Birchwood M, Patterson P, Juckel G, Heinz A, et al. 2010. Prediction of psychosis in adolescents and young adults at high risk: results from the prospective European prediction of psychosis study. Arch Gen Psychiatry. 67:241-251.
41. Salisbury DF, Kuroki N, Kasai K, Shenton ME, McCarley RW. 2007. Progressive and interrelated functional and structural evidence for post-onset brain reduction in schizophrenia. Arch Gen Psychiatry. 64:521-529.
42. Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC. 1998. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry. 59(Suppl. 20):22-33. quiz 34-57.
43. Sohal VS, Zhang F, Yizhar O, Deisseroth K. 2009. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature. 459:698-702.
44. Sowell ER, Peterson BS, Thompson PM, Welcome SE, Henkenius AL, Toga AW. 2003. Mapping cortical change across the human life span. Nat Neurosci. 6:309-315.
45. Spencer KM, Salisbury DF, Shenton ME, McCarley RW. 2008. Gamma-band auditory steady-state responses are impaired in first episode psychosis. Biol Psychiatry. 64:369-375.
46. 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.
47. Takahashi T, Wood SJ, Yung AR, Soulsby B, McGorry PD, Suzuki M, Kawasaki Y, Phillips LJ, Velakoulis D, Pantelis C. 2009. Progressive gray matter reduction of the superior temporal gyrus during transition to psychosis. Arch Gen Psychiatry. 66:366-376.
48. Teale P, Collins D, Maharajh K, Rojas DC, Kronberg E, Reite M. 2008. Cortical source estimates of gamma band amplitude and phase are different in schizophrenia. Neuroimage. 42:1481-1489.
49. Tsuchimoto R, Kanba S, Hirano S, Oribe N, Ueno T, Hirano Y, Nakamura I, Oda Y, Miura T, Onitsuka T. 2011. Reduced high and low frequency gamma synchronization in patients with chronic schizophrenia. Schizophr Res. 133:99-105.
50. Uhlhaas PJ, Roux F, Singer W, Haenschel C, Sireteanu R, Rodriguez E. 2009. The development of neural synchrony reflects late maturation and restructuring of functional networks in humans. Proc Natl Acad Sci USA. 106:9866-9871.
51. Uhlhaas PJ, Singer W. 2010. Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci. 11:100-113.
52. Uhlhaas PJ, Singer W. 2011. The development of neural synchrony and large-scale cortical networks during adolescence: relevance for the pathophysiology of schizophrenia and neurodevelopmental hypothesis. Schizophr Bull. 37:514-523.
53. Vierling-Claassen D, Siekmeier P, Stufflebeam S, Kopell N. 2008. Modeling GABA alterations in schizophrenia: a link between impaired inhibition and altered gamma and beta range auditory entrainment. J Neurophysiol. 99:2656-2671.
54. Vohs JL, Chambers RA, O'Donnell BF, Krishnan GP, Morzorati SL. 2012. Auditory steady state responses in a schizophrenia rat model probed by excitatory/inhibitory receptor manipulation. Int J Psychophysiol. 86:136-142.
55. Wilson TW, Hernandez OO, Asherin RM, Teale PD, Reite ML, Rojas DC. 2008. Cortical gamma generators suggest abnormal auditory circuitry in early-onset psychosis. Cereb Cortex. 18:371-378.