Progressive decrease of left Heschl gyrus and planum temporale gray matter volume in first-episode schizophrenia: A longitudinal magnetic resonance imaging study

Archives of General Psychiatry

Volumn 60, Issue 8, 2003, Pages 766-775

  Kasai, Kiyoto ^a,b   Shenton, Martha E ^a,b,c   Salisbury, Dean F ^a,b,d   Hirayasu, Yoshio ^e   Onitsuha, Toshiaki ^a,b   Spencer, Magdalena H ^a,b   Yurgelun Todd, Deborah A ^d   Kikinis, Ron ^c   Jolesz, Ferenc A ^c   McCarley, Robert W ^a,b  

^a VA Clinical Neuroscience Division   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d MCLEAN HOSPITAL   (United States)

^e KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AFFECTIVE PSYCHOSIS; ARTICLE; AUDITORY CORTEX; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GRAY MATTER; HEARING; HESCHL GYRUS; HUMAN; LANGUAGE; MALE; MANIC PSYCHOSIS; NEOCORTEX; NUCLEAR MAGNETIC RESONANCE IMAGING; PSYCHOSIS; SCHIZOPHRENIA; TEMPORAL LOBE;

ADOLESCENT; ADULT; ATROPHY; AUDITORY CORTEX; BIPOLAR DISORDER; CEREBRAL CORTEX; DEPRESSIVE DISORDER, MAJOR; DOMINANCE, CEREBRAL; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; MATHEMATICAL COMPUTING; PROSPECTIVE STUDIES; REFERENCE VALUES; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY; TEMPORAL LOBE;

EID: 0041653565     PISSN: 0003990X     EISSN: None     Source Type: Journal    
DOI: 10.1001/archpsyc.60.8.766     Document Type: Article

References (70)

1. Zattore RJ, Binder JR. Functional and structural imaging of the human auditory system. In: Toga AW, Mazziotta JC, eds. Brain Mapping: The Systems. San Diego, Calif: Academic Press; 2000:365-402.
2. Pearlson GD. Superior temporal gyrus and planum temporale in schizophrenia: a selective review. Prog Neuropsychopharmacol Biol Psychiatry. 1997;21:1203-1229.
3. Mesulam MM. Behavioral neuroanatomy. In: Mesulam MM, Principles of Behavioral and Cognitive Neurology. New York, NY: Oxford University Press; 2000:1-120.
4. Geschwind N, Levitsky W. Human brain: left-right asymmetries in temporal speech region. Science. 1968;161:186-187.
5. Galaburda AM, Sanides F, Geschwind N. Human brain: cytoarchitectonic left-right asymmetries in the temporal speech region. Arch Neurol. 1978;35:812-817.
6. Javitt DO. Psychophysiology of schizophrenia. Curr Opin Psychiatry. 1997;10:11-15.
7. Light GA, Braff DL. Human and animal studies of schizophrenia-related gating deficits. Curr Psychiatry Rep. 1999;1:31-40.
8. McCarley RW, Niznikiewicz MA, Salisbury DF, Nestor PG, O'Donnell BF, Hirayasu Y, Grunze H, Greene RW, Shenton ME. Cognitive dysfunction in schizophrenia: unifying basic research and clinical aspects. Eur Arch Psychiatry Clin Neurosci. 1999;249(suppl 4):69-82.
9. Rojas DC, Teale P, Sheeder J, Simon J, Reite M. Sex-specific expression of Heschl's gyrus functional and structural abnormalities in paranoid schizophrenia. Am J Psychiatry. 1997;154:1655-1662.
10. Hirayasu Y, McCarley RW, Salisbury DF, Tanaka S, Kwon JS, Frumin M, Snyderman D, Yurgelun-Todd D, Kikinis R, Jolesz FA, Shenton ME. Planum temporale and Heschl gyrus volume reduction in schizophrenia. Arch Gen Psychiatry. 2000;57:692-699.
11. Petty RG, Barta PE, Pearlson GO, McGilchrist IK, Lewis RW, Tien AY, Pulver A, Vaughn DD, Casanova MF, Powers RE. Reversal of asymmetry of the planum temporale in schizophrenia. Am J Psychiatry. 1995;152:715-721.
12. Kulynych JJ, Vladar K, Fantie BD, Jones DW, Weinberger DR. Normal asymmetry of the planum temporale in patients with schizophrenia: three-dimensional cortical morphometry with MRI. Br J Psychiatry. 1995;166:742-749.
13. Barta PE, Pearlson GD, Brill LB II, Royall R, McGilchrist IK, Pulver AE, Powers RE, Casanova MF, Tien AY, Frangou S, Petty RG. Planum temporale asymmetry reversal in schizophrenia: replication and relationship to gray matter abnormalities. Am J Psychiatry. 1997;154:661-667.
14. Frangou S, Sharma T, Sigmudsson T, Barta P, Pearlson G, Murray RM. The Maudsley family study 4: normal planum temporale asymmetry in familial schizophrenia: a volumetric MRI study. Br J Psychiatry. 1997;170:328-333.
15. Kwon JS, McCarley RW, Hirayasu Y, Anderson JE, Fischer IA, Kikinis R, Jolesz FA, Shenton ME. Left planum temporale volume reduction in schizophrenia. Arch Gen Psychiatry. 1999;56:142-148.
16. Kropotov JD, Näätänen R, Sevostianov AV, Alho K, Reinikainen K, Kropotova OV. Mismatch negativity to auditory stimulus change recorded directly from the human temporal cortex. Psychophysiology. 1995;32:418-422.
17. Shelley AM, Ward PB, Catts SV, Michie PT, Andrews S, McConaghy N. Mismatch negativity: an index of a preattentive processing deficit in schizophrenia. Biol Psychiatry. 1991;30:1059-1062.
18. Javitt DC, Doneshka P, Grochowski S, Ritter W. Impaired mismatch negativity generation reflects widespread dysfunction of working memory in schizophrenia. Arch Gen Psychiatry. 1995;52:550-558.
19. Salisbury DF, Shenton ME, Griggs CB, Bonner-Jackson A, McCarley RW. Mismatch negativity in chronic schizophrenia and first-episode schizophrenia. Arch Gen Psychiatry. 2002;59:686-694.
20. Wible CG, Kubicki M, Yoo SS, Kacher DF, Salisbury DF, Anderson MC, Shenton ME, Hirayasu Y, Kikinis R, Jolesz FA, McCarley RW. A functional magnetic resonance imaging study of auditory mismatch in schizophrenia. Am J Psychiatry. 2001;158:938-943.
21. Dierks T, Linden DEJ, Jandl M, Formisano E, Goebel R, Lanfermann H, Singer W. Activation of Heschi's gyrus during auditory hallucinations. Neuron. 1999;22:615-622.
22. Shapleske J, Rossell SL, Simmons A, David AS, Woodruff PWR. Are auditory hallucinations the consequence of abnormal cerebral lateralization? a morphometric MRI study of the sylvian fissure and planum temporale. Biol Psychiatry. 2001;49:685-693.
23. Rossi A, Serio A, Stratta P, Petruzzi C, Schiazza G, Mancini F, Casacchia M. Planum temporale asymmetry and thought disorder in schizophrenia. Schizophr Res. 1994;12:1-7.
24. DeLisi LE, Hoff AL, Neale C, Kushner M. Asymmetries in the superior temporal lobe in male and female first-episode schizophrenic patients: measures of the planum temporale and superior temporal gyrus by MRI. Schizophr Res. 1994;12:19-28.
25. Kleinschmidt A, Falkai P, Huang Y, Schneider T, Furst G, Steinmetz H. In vivo morphometry of planum temporale asymmetry in first-episode schizophrenia. Schizophr Res. 1994;12:9-18.
26. Knight RT, Scabini D, Woods DL, Clayworth CC. Contributions of temporal parietal junction to the human auditory P3. Brain Res. 1989;502:109-116.
27. Ford JM. Schizophrenia: the broken P300 and beyond. Psychophysiology. 1999;36:667-682.
28. O'Donnell BF, McCarley RW, Potts GF, Salisbury DF, Nestor PG, Hirayasu Y, Niznikiewicz MA, Barnard J, Shen ZJ, Weinstein DM, Bookstein FL, Shenton ME. Identification of neural circuits underlying P300 abnormalities in schizophrenia. Psychophysiology. 1999;36:388-398.
29. McCarley RW, Shenton ME, O'Donnell BF, Faux SF, Kikinis R, Nestor PG, Jolesz FA. Auditory P300 abnormalities and left posterior temporal gyrus volume reduction in schizophrenia. Arch Gen Psychiatry. 1993;50:190-197.
30. McCarley RW, Salisbury DF, Hirayasu Y, Yurgelun-Todd DA, Tohen M, Zarate C, Kikinis R, Jolesz FA, Shenton ME. Association between smaller left posterior superior temporal gyrus MRI volume and smaller left temporal P300 amplitude in first episode schizophrenia. Arch Gen Psychiatry. 2002;59:321-331.
31. O'Donnell BF, Faux SF, McCarley RW, Kimble MO, Salisbury DF, Nestor PG, Kikinis R, Jolesz FA, Shenton ME. Increased rate of P300 latency prolongation with age in schizophrenia. Arch Gen Psychiatry. 1995;52:544-549.
32. Mathalon DH, Ford JM, Rosenbloom M, Pfefferbaum A. P300 reduction and prolongation with illness duration in schizophrenia. Biol Psychiatry. 2000;47:413-427.
33. Shenton ME, Kikinis R, Jolesz FA, Pollak SD, LeMay M, Wible CG, Hokama H, Martin J, Metcalf D, Coleman M, McCarley RW. Abnormalities of the left temporal lobe and thought disorder in schizophrenia: a quantitative magnetic resonance imaging study. N Engl J Med. 1992;327:604-612.
34. Kircher TTJ, Liddle PF, Brammer MJ, Williams S, Murray RM, McGuire PK. Neural correlates of formal thought disorder in schizophrenia: preliminary findings from a functional magnetic resonance imaging study. Arch Gen Psychiatry. 2001;58:769-774.
35. Mathalon DH, Sullivan EV, Lim KO, Pfefferbaum A. Progressive brain volume changes and the clinical course of schizophrenia in men: a longitudinal magnetic resonance imaging study. Arch Gen Psychiatry. 2001;58:148-157.
36. Hirayasu Y, Shenton ME, Salisbury DF, Frumin M, Fischer IA, Farrell D, Yurgelun-Todd DA, Zarate C, McCarley RW. Progressive change in posterior superior temporal gyrus in schizophrenia. Biol Psychiatry. 1999;45:117S.
37. Kasai K, Shenton ME, Salisbury DF, Hirayasu Y, Lee CU, Ciszewski AA, Yurgelun-Todd DA, Kikinis R, Jolesz FA, McCarley RW. Progressive decrease of left superior temporal gyrus gray matter volume in patients with first-episode schizophrenia. Am J Psychiatry. 2003;160:156-164.
38. Keshavan MS, Haas GL, Kahn CE, Aguilar E, Dick EL, Schooler NR, Sweeney JA, Pettegrew JW. Superior temporal gyrus and the course of early schizophrenia: progressive, static, or reversible? J Psychiatr Res. 1998;32:161-167.
39. Oldfield RC. The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia. 1971;9:97-113.
40. Hollingshead AB. Two Factor Index of Social Position. New Haven, Conn: Yale University Press; 1965.
41. Hirayasu Y, Shenton ME, Salisbury DF, Dickey CC, Fisher IA, Mazzoni P, Kisler T, Aarakaki H, Kwon JS, Anderson JE, Yurgelun-Todd D, Tohen M, McCarley RW. Lower left temporal lobe MR volumes in patients with first-episode schizophrenia compared with psychotic patients with first-episode affective disorder and normal subjects. Am J Psychiatry. 1998;155:1384-1391.
42. Hirayasu Y, Shenton ME, Salisbury DF, Kwon JS, Wible CG, Fischer IA, Yurgelun-Todd D, Zarate C, Kikinis R, Jolesz FA, McCarley RW. Subgenual cingulate cortex volume in first-episode psychosis. Am J Psychiatry. 1999;156:1091-1093.
43. Hirayasu Y, Tanaka S, Shenton ME, Salisbury DF, DeSantis MA, Levitt JJ, Wible C, Yurgelun-Todd D, Kikinis R, Jolesz FA, McCarley RW. Prefrontal gray matter volume reduction in first-episode schizophrenia. Cereb Cortex. 2001;11:374-381.
44. Salisbury DF, Shenton ME, Sherwood AR, Fischer IA, Yurgelun-Todd DA, Tohen M, McCarley RW. First-episode schizophrenic psychosis differs from first-episode affective psychosis and controls in P300 amplitude over left temporal lobe. Arch Gen Psychiatry. 1998;55:173-180.
45. Lee CU, Shenton ME, Salisbury DF, Kasai K, Onitsuka T, Dickey CC, Yurgelun-Todd D, Kikinis R, Jolesz FA, McCarley RW. Fusiform gyrus volume reduction in first-episode schizophrenia: an MRI study. Arch Gen Psychiatry. 2002;59:775-781.
46. Spitzer RL, Williams JBW, Gibbson M, First M. The Structured Clinical Interview for DSM-III-R Non-Patient Edition (SCID-NP). Washington, DC: American Psychiatric Association; 1990.
47. Spitzer RL, Williams JBW, Gibbson M, First M. The Structured Clinical Interview for DSM-III-R (SCID). Washington, DC: American Psychiatric Association; 1990.
48. DeLisi LE, Sakuma M, Tew W, Kushner M, Hoff AL, Grimson R. Schizophrenia as a chronic active brain process: a study of progressive brain structural change subsequent to the onset of schizophrenia. Psychiatry Res. 1997;74:129-140.
49. Lieberman JA, Chakos M, Wu H, Aivir J, Hoffman E, Robinson D, Bilder R. Longitudinal study of brain morphology in first episode schizophrenia. Biol Psychiatry. 2001;49:487-499.
50. Folstein MF, Folstein SE, McHugh PR. "Mini-Mental State": a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189-198.
51. Wechsler D. Wechsler Adult Intelligence Scale-Revised. New York, NY: Harcourt Brace Jovanovich Inc; 1981.
52. Endicott J, Spitzer RL, Fleiss JL, Cohen J. The global assessment scale: a procedure for measuring overall severity of psychiatric disturbance. Arch Gen Psychiatry. 1976;33:766-771.
53. Overall JE, Hollister LE, Pichot P. Major psychiatric disorders: a four-dimensional model. Arch Gen Psychiatry. 1967;16:146-151.
54. Overall JE, Gorham DR. The Brief Psychiatric Rating Scale. Psychol Rep. 1962;10:799-812.
55. Wible CG, Shenton ME, Hokama H, Kikinis R, Jolesz FA, Metcalf D, McCarley RW. Prefrontal cortex and schizophrenia: a quantitative magnetic resonance imaging study. Arch Gen Psychiatry. 1995;52:279-288.
56. Gerig G, Kubler O, Kikinis R, Jolesz FA. Nonlinear anisotropic filtering of MRI data. IEEE Trans Med Imaging. 1992;11:221-232.
57. Wells WM III, Grimson WEL, Kikinis R, Jolesz FA. Adaptive segmentation of MRI data. IEEE Trans Med Imaging. 1996;15:429-442.
58. Steinmetz H, Rademacher J, Huang Y, Hefter H, Zilles K, Thron A, Freund HJ. Cerebral asymmetry: MR planimetry of the human planum temporale. J Comput Assist Tomogr. 1989;13:996-1005.
59. Barta PE, Petty RG, McGilchrist I, Lewis RW, Jerram M, Casanova MF, Powers RE, Brill LB II, Pearlson GD. Asymmetry of the planum temporale: methodological considerations and clinical associations. Psychiatry Res. 1995;61:137-150.
60. Honeycutt NA, Musick A, Barta PE, Pearlson GD. Measurement of the planum temporale (PT) on magnetic resonance imaging scans: temporal PT alone and with parietal extension. Psychiatry Res. 2000;98:103-116.
61. Mojtabai R, Bromet EJ, Harvey P, Carlson GA, Craig TJ, Fennig S. Neuropsychological differences between first-admission schizophrenia and psychotic affective disorders. Am J Psychiatry. 2000;157:1453-1460.
62. Seidman LJ, Kremen WS, Koren D, Faraone SV, Goldstein JM, Tsuang MT. A comparative profile analysis of neuropsychological functioning in patients with schizophrenia and bipolar psychoses. Schizophr Res. 2002;53:31-44.
63. Coyle JT. The glutamatergic dysfunction hypothesis for schizophrenia. Harv Rev Psychiatry. 1996;3:241-253.
64. McCarley RW, Hsiao JK, Freedman R, Pfefferbaum A, Donchin E. Neuroimaging and the cognitive neuroscience of schizophrenia. Schizophr Bull. 1996;22:703-25.
65. McCarley RW, Wible CG, Frumin M, Hirayasu Y, Levitt JJ, Fischer IA, Shenton ME. MRI anatomy of schizophrenia. Biol Psychiatry. 1999;45:1099-1119.
66. Seldon H. Structure of human auditory cortex, I: cytoarchitectonics and dendritic distributions. Brain Res. 1981;229:277-294.
67. Seldon H. Structure of human auditory, cortex, II: axon distributions and morphological correlates of speech perception. Brain Res. 1981;229:295-310.
68. Seldon H. Structure of human auditory cortex, III: statistical analysis of denritic trees. Brain Res. 1982;249:211-221.
69. Hutsler J, Gazzaniga M. Acetylcholinesterase staining in human auditory and language cortices: regional variation of structural features. Cereb Cortex. 1996;6:260-270.
70. Hollinger DP, Galaburda AM, Harrison PJ. Cerebral asymmetry. In: Harrison PJ, Roberts GW, eds. The Neuropathology of Schizophrenia. New York, NY: Oxford University Press; 2000:151-171.