Auditory cortex asymmetry, altered minicolumn spacing and absence of ageing effects in schizophrenia.

The superior temporal gyrus, which contains the auditory cortex, including the planum temporale, is the most consistently altered neocortical structure in schizophrenia (Shenton ME, Dickey CC, Frumin M, McCarley RW. A review of MRI findings in schizophrenia. Schizophr Res 2001; 49: 1-52). Auditory hallucinations are associated with abnormalities in this region and activation in Heschl's gyrus. Our review of 34 MRI and 5 post-mortem studies of planum temporale reveals that half of those measuring region size reported a change in schizophrenia, usually consistent with a reduction in the left hemisphere and a relative increase in the right hemisphere. Furthermore, female subjects are under-represented in the literature and insight from sex differences may be lost. Here we present evidence from post-mortem brain (N = 21 patients, compared with 17 previously reported controls) that normal age-associated changes in planum temporale are not found in schizophrenia. These age-associated differences are reported in an adult population (age range 29-90 years) and were not found in the primary auditory cortex of Heschl's gyrus, indicating that they are selective to the more plastic regions of association cortex involved in cognition. Areas and volumes of Heschl's gyrus and planum temporale and the separation of the minicolumns that are held to be the structural units of the cerebral cortex were assessed in patients. Minicolumn distribution in planum temporale and Heschl's gyrus was assessed on Nissl-stained sections by semi-automated microscope image analysis. The cortical surface area of planum temporale in the left hemisphere (usually asymmetrically larger) was positively correlated with its constituent minicolumn spacing in patients and controls. Surface area asymmetry of planum temporale was reduced in patients with schizophrenia by a reduction in the left hemisphere (F = 7.7, df 1,32, P < 0.01). The relationship between cortical asymmetry and the connecting, interhemispheric callosal white matter was also investigated; minicolumn asymmetry of both Heschl's gyrus and planum temporale was correlated with axon number in the wrong subregions of the corpus callosum in patients. The spacing of minicolumns was altered in a sex-dependent manner due to the absence of age-related minicolumn thinning in schizophrenia. This is interpreted as a failure of adult neuroplasticity that maintains neuropil space. The arrested capacity to absorb anomalous events and cognitive demands may confer vulnerability to schizophrenic symptoms when adult neuroplastic demands are not met.

[1]  R. Guillery Is postnatal neocortical maturation hierarchical? , 2005, Trends in Neurosciences.

[2]  Robin M. Murray,et al.  The Maudsley Family Study 4. Normal planum temporale asymmetry in familial schizophrenia , 1997, British Journal of Psychiatry.

[3]  Normal planum temporale asymmetry in familial schizophrenia: A volumetric MRI study , 1996, Schizophrenia Research.

[4]  T. Crow,et al.  The cytoarchitecture of sulcal folding in Heschl’s sulcus and the temporal cortex in the normal brain and schizophrenia: lamina thickness and cell density , 2004, Neuroscience Letters.

[5]  T. Crow,et al.  Reduced density of calbindin-immunoreactive interneurons in the planum temporale in schizophrenia , 2005, Brain Research.

[6]  L. Penrose Survey of cases of familial mental illness , 2005, European Archives of Psychiatry and Clinical Neuroscience.

[7]  Douglas W. Jones,et al.  Three‐Dimensional Surface Rendering in MRI Morphometry: A Study of the Planum Temporale , 1993, Journal of computer assisted tomography.

[8]  Nikos Makris,et al.  Neuroanatomic substrates of sex differences in language dysfunction in schizophrenia: A pilot study , 2007, Schizophrenia Research.

[9]  R Kikinis,et al.  Left planum temporale volume reduction in schizophrenia. , 1999, Archives of general psychiatry.

[10]  N. Andreasen,et al.  Left hemisphere language dominance in schizophrenic patients and normal controls: A study of anatomical and functional asymmetries , 1995, Schizophrenia Research.

[11]  A. Galaburda,et al.  A 3D MRI study of the planum temporale in schizophrenia , 1995, Schizophrenia Research.

[12]  S. Chance Subtle Changes in the Ageing Human Brain , 2006, Nutrition and health.

[13]  P. Falkai,et al.  In vivo morphometry of planum temporale asymmetry in first-episode schizophrenia , 1994, Schizophrenia Research.

[14]  N. Makris,et al.  Impact of normal sexual dimorphisms on sex differences in structural brain abnormalities in schizophrenia assessed by magnetic resonance imaging. , 2002, Archives of general psychiatry.

[15]  A. Schleicher,et al.  Human brain growth in the 19th and 20th century , 1979, Journal of the Neurological Sciences.

[16]  T. Crow,et al.  Minicolumn thinning in temporal lobe association cortex but not primary auditory cortex in normal human ageing , 2006, Acta Neuropathologica.

[17]  G D Pearlson,et al.  Reversal of asymmetry of the planum temporale in schizophrenia. , 1995, The American journal of psychiatry.

[18]  J. Winn,et al.  Brain , 1878, The Lancet.

[19]  C. C. Castro,et al.  Rightward cerebral asymmetry in subtypes of schizophrenia according to Leonhard's classification and to DSM-IV: a structural MRI study , 2003, Psychiatry Research: Neuroimaging.

[20]  Todd S. Woodward,et al.  Brain activation mediates the association between structural abnormality and symptom severity in schizophrenia , 2007, NeuroImage.

[21]  J. Hogg Magnetic resonance imaging. , 1994, Journal of the Royal Naval Medical Service.

[22]  B. Pakkenberg,et al.  Neocortical neuron number in humans: Effect of sex and age , 1997, The Journal of comparative neurology.

[23]  P. Rakic A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution , 1995, Trends in Neurosciences.

[24]  R. McCarley,et al.  A review of MRI findings in schizophrenia , 2001, Schizophrenia Research.

[25]  R. M. Murray,et al.  Normal planum temporale asymmetry in familial schizophrenia: a volumetric MRI study , 1997, Psychiatry Research: Neuroimaging.

[26]  Helen L Jamison,et al.  Hemispheric specialization for processing auditory nonspeech stimuli. , 2006, Cerebral cortex.

[27]  T. J. Crow,et al.  Minicolumnar structure in Heschl’s gyrus and planum temporale: Asymmetries in relation to sex and callosal fiber number , 2006, Neuroscience.

[28]  D. Kelly,et al.  Minicolumnar organization within somatosensory cortical segregates: II. Emergent functional properties. , 1994, Cerebral cortex.

[29]  N. Andreasen,et al.  Regional cerebral blood flow (rCBF) within heschl's gyrus and the planum temporale in schizophrenic patients and controls during language tasks: An MRI and pet study , 1995, Schizophrenia Research.

[30]  P. K. McGuire,et al.  Anomalous Cerebral Asymmetry in Patients with Schizophrenia Demonstrated by Voxel-Based Morphometry , 2008, Biological Psychiatry.

[31]  C. Economo,et al.  Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen , 1925 .

[32]  P. Teale,et al.  Sex-specific expression of Heschl's gyrus functional and structural abnormalities in paranoid schizophrenia. , 2015, The American journal of psychiatry.

[33]  G. Smith,et al.  Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen. , 1927 .

[34]  H. Möller,et al.  Does the definition of borders of the planum temporale influence the results in schizophrenia? , 2002, The American journal of psychiatry.

[35]  R. Murray,et al.  Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. , 2000, Archives of general psychiatry.

[36]  Yasuhiro Kawasaki,et al.  Morphologic alterations of the parcellated superior temporal gyrus in schizophrenia spectrum , 2006, Schizophrenia Research.

[37]  Neurology and Neurobiology , 1990 .

[38]  MRI measures of auditory cortex area correlate with an ERP index of auditory sensory memory in schizophrenia , 1995, Schizophrenia Research.

[39]  G D Pearlson,et al.  Planum temporale asymmetry reversal in schizophrenia: replication and relationship to gray matter abnormalities. , 1997, The American journal of psychiatry.

[40]  D. Kelly,et al.  Minicolumnar organization within somatosensory cortical segregates: I. Development of afferent connections. , 1994, Cerebral cortex.

[41]  T. Crow,et al.  Ventricular enlargement in schizophrenia: a primary change in the temporal lobe? , 2003, Schizophrenia Research.

[42]  David A Lewis,et al.  Reduced Pyramidal Cell Somal Volume in Auditory Association Cortex of Subjects with Schizophrenia , 2003, Neuropsychopharmacology.

[43]  V H Denenberg,et al.  A developmental study of sex and age interactions in the human corpus callosum. , 1992, Brain research. Developmental brain research.

[44]  K. Nuechterlein,et al.  Electrodermal measures in schizophrenia: Episode or vulnerability indicators? , 1989, Schizophrenia Research.

[45]  A. Simmons,et al.  Are auditory hallucinations the consequence of abnormal cerebral lateralization? A morphometric MRI study of the sylvian fissure and planum temporale , 2001, Biological Psychiatry.

[46]  Karl J. Friston,et al.  Schizophrenia: a disconnection syndrome? , 1995, Clinical neuroscience.

[47]  N. Andreasen,et al.  Morphometry of the superior temporal plane in schizophrenia: relationship to clinical correlates. , 2004, The Journal of neuropsychiatry and clinical neurosciences.

[48]  Wolfgang Grodd,et al.  Mismatch negativity responses in schizophrenia: a combined fMRI and whole-head MEG study. , 2004, The American journal of psychiatry.

[49]  Ron Kikinis,et al.  Association between smaller left posterior superior temporal gyrus volume on magnetic resonance imaging and smaller left temporal P300 amplitude in first-episode schizophrenia. , 2002, Archives of general psychiatry.

[50]  Norbert Kathmann,et al.  In-vivo analysis of the human planum temporale (PT): does the definition of PT borders influence the results with regard to cerebral asymmetry and correlation with handedness? , 2001, Psychiatry Research: Neuroimaging.

[51]  Paul Leonard Gabbott Radial organisation of neurons and dendrites in human cortical areas 25, 32, and 32′ , 2003, Brain Research.

[52]  T. Arendt Neurodegeneration and plasticity , 2004, International Journal of Developmental Neuroscience.

[53]  James J. Levitt,et al.  An MRI study of spatial probability brain map differences between first-episode schizophrenia and normal controls , 2004, NeuroImage.

[54]  Nicolette Marshall,et al.  Temporal lobe abnormalities in first-episode psychosis. , 2002, The American journal of psychiatry.

[55]  Ron Kikinis,et al.  Progressive decrease of left Heschl gyrus and planum temporale gray matter volume in first-episode schizophrenia: a longitudinal magnetic resonance imaging study. , 2003, Archives of general psychiatry.

[56]  G. Pearlson,et al.  Medial and superior temporal gyral volumes and cerebral asymmetry in schizophrenia versus bipolar disorder , 1997, Biological Psychiatry.

[57]  P. Stratta,et al.  Planum temporale in schizophrenia: a magnetic resonance study , 1992, Schizophrenia Research.

[58]  F. Benes,et al.  The density of pyramidal and nonpyramidal neurons in anterior cingulate cortex of schizophrenic and bipolar subjects , 2001, Biological Psychiatry.

[59]  Y. Hirayasu,et al.  Reduced planum temporale volume and delusional behaviour in patients with schizophrenia , 2007, European Archives of Psychiatry and Clinical Neuroscience.

[60]  M G Rosa,et al.  Cellular heterogeneity in cerebral cortex: A study of the morphology of pyramidal neurones in visual areas of the marmoset monkey , 1999, The Journal of comparative neurology.

[61]  T. Crow,et al.  The size and fibre composition of the corpus callosum with respect to gender and schizophrenia: a post-mortem study. , 1999, Brain : a journal of neurology.

[62]  J. Rybakowski,et al.  [Gender differences in schizophrenia]. , 1992, Psychiatria polska.

[63]  Y. Kawasaki,et al.  Volume reduction of the left planum temporale gray matter associated with long duration of untreated psychosis in schizophrenia: A preliminary report , 2007, Psychiatry Research: Neuroimaging.

[64]  D. Jeste,et al.  Late onset non-affective endogenous psychosis. A report from India , 1989, Schizophrenia Research.

[65]  R. McCarley,et al.  Progressive and interrelated functional and structural evidence of post-onset brain reduction in schizophrenia. , 2007, Archives of general psychiatry.

[66]  Douglas W. Jones,et al.  Morphometry: A study of the planum temporale , 1993 .

[67]  L. DeLisi,et al.  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 , 1994, Schizophrenia Research.

[68]  R. Kahn,et al.  Handedness, language lateralisation and anatomical asymmetry in schizophrenia: meta-analysis. , 2001, The British journal of psychiatry : the journal of mental science.

[69]  L. Penrose Survey of cases of familial mental illness. L. S. Penrose, July 1945. , 1991, European archives of psychiatry and clinical neuroscience.

[70]  D. Weinberger,et al.  Normal Asymmetry of the Planum Temporale in Patients with Schizophrenia , 1995, British Journal of Psychiatry.

[71]  M. Miller,et al.  Region‐of‐interest‐based analysis with application of cortical thickness variation of left planum temporale in schizophrenia and psychotic bipolar disorder , 2008, Human brain mapping.

[72]  Manuel F. Casanova,et al.  Mean cell spacing abnormalities in the neocortex of patients with schizophrenia , 2005, Psychiatry Research.

[73]  Miki Uetsuki,et al.  Abnormal association between reduced magnetic mismatch field to speech sounds and smaller left planum temporale volume in schizophrenia , 2004, NeuroImage.

[74]  H. Seldon,et al.  The left human speech-processing cortex is thinner but longer than the right , 2003, Laterality.

[75]  A. Toga,et al.  Mapping brain maturation , 2006, Trends in Neurosciences.

[76]  R. Kikinis,et al.  Planum temporale and Heschl gyrus volume reduction in schizophrenia: a magnetic resonance imaging study of first-episode patients. , 2000, Archives of general psychiatry.

[77]  T. Sharma,et al.  Unreality symptoms and volumetric measures of Heschl’s gyrus and planum temporal in first-episode psychosis , 2005, Biological Psychiatry.

[78]  J. Kornhuber,et al.  Cortical activity associated with auditory hallucinations , 2004, Neuroreport.

[79]  T. Crow,et al.  Anomalous asymmetry of fusiform and parahippocampal gyrus gray matter in schizophrenia: A postmortem study. , 2000, The American journal of psychiatry.

[80]  Peter Falkai,et al.  Disturbed planum temporale asymmetry in schizophrenia. A quantitative post-mortem study , 1995, Schizophrenia Research.

[81]  M. LeMay,et al.  Abnormalities of the left temporal lobe and thought disorder in schizophrenia. A quantitative magnetic resonance imaging study. , 1992, The New England journal of medicine.

[82]  B. Dean,et al.  Serotonin2A receptors are reduced in the planum temporale from subjects with schizophrenia , 2000, Schizophrenia Research.

[83]  A. David,et al.  The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance , 1999, Brain Research Reviews.

[84]  T. J. Crow,et al.  Schizophrenia as a transcallosal misconnection syndrome , 1998, Schizophrenia Research.

[85]  R Kikinis,et al.  Auditory P300 abnormalities and left posterior superior temporal gyrus volume reduction in schizophrenia. , 1993, Archives of general psychiatry.

[86]  W. Bilker,et al.  Long-term course of hospitalization for schizophrenia: Part II. Change with passage of time. , 1992, Schizophrenia bulletin.

[87]  Daniel S. O'Leary,et al.  An MRI-Based Parcellation Method for the Temporal Lobe , 2000, NeuroImage.

[88]  Alessandro Rossi,et al.  Planum temporale asymmetry and thought disorder in schizophrenia , 1994, Schizophrenia Research.

[89]  Sabine Landau,et al.  Evidence for altered neuronal organisation within the planum temporale in major psychiatric disorders , 2005, Schizophrenia Research.

[90]  A Capdevila,et al.  When does human brain development end? Evidence of corpus callosum growth up to adulthood , 1993, Annals of neurology.