Schizophrenia, neurodevelopment and corpus callosum

The Zeitgeist favors an interpretation of schizophrenia as a condition of abnormal connectivity of cortical neurons, particularly in the prefrontal and temporal cortex. The available evidence points to reduced connectivity, a possible consequence of excessive synaptic pruning in development. A decreased thalamic input to the cerebral cortex appears likely, and developmental studies predict that this decrease should entail a secondary loss of both long- and short-range cortico-cortical connections, including connections between the hemispheres. Indeed, morphological, electrophysiological and neuropsychological studies over the last two decades suggest that the callosal connections are altered in schizophrenics. However, the alterations are subtle and sometimes inconsistent across studies, and need to be investigated further with new methodologies.

[1]  L. Glantz,et al.  Reduction of synaptophysin immunoreactivity in the prefrontal cortex of subjects with schizophrenia. Regional and diagnostic specificity. , 1997, Archives of general psychiatry.

[2]  P. Bovet,et al.  Autism in schizophrenia revisited. , 1991, Comprehensive psychiatry.

[3]  J. Parnas,et al.  High-risk studies and neurodevelopmental hypothesis , 2002 .

[4]  J Bullier,et al.  Structural basis of cortical synchronization. II. Effects of cortical lesions. , 1995, Journal of neurophysiology.

[5]  Joseph T. Wells Timing Is of the Essence , 2001 .

[6]  H. Killackey,et al.  The ontogeny of the distribution of callosal projection neurons in the rat parietal cortex , 1981, The Journal of comparative neurology.

[7]  E. Stransky,et al.  Zur Auffassung Gewisser Symptome der Dementia Praecox , 1905 .

[8]  J. Bradshaw,et al.  Bimanual Coordination in Chronic Schizophrenia , 2001, Brain and Cognition.

[9]  P. Goldman-Rakic,et al.  Abnormally high neuronal density in the schizophrenic cortex. A morphometric analysis of prefrontal area 9 and occipital area 17. , 1995, Archives of general psychiatry.

[10]  Brent B. Stanfield,et al.  Selective collateral elimination in early postnatal development restricts cortical distribution of rat pyramidal tract neurones , 1982, Nature.

[11]  K. Nuechterlein,et al.  Cortical oscillations and schizophrenia: timing is of the essence. , 1999, Archives of general psychiatry.

[12]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[13]  S. Skare,et al.  Abnormal brain white matter in schizophrenia: a diffusion tensor imaging study , 2001, Neuroreport.

[14]  J. Kleinman,et al.  Abnormal excitatory neurotransmitter metabolism in schizophrenic brains. , 1995, Archives of general psychiatry.

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

[16]  E. Ross,et al.  Topography of the Human Corpus Callosum , 1985, Journal of neuropathology and experimental neurology.

[17]  A. David Stroop effects within and between the cerebral hemispheres: Studies in normals and acallosals , 1992, Neuropsychologia.

[18]  N. Thakor,et al.  The nonlinear dynamical analysis of the EEG in schizophrenia with temporal and spatial embedding dimension. , 2001, Journal of medical engineering & technology.

[19]  T. Crow Schizophrenia as the price that Homo sapiens pays for language: a resolution of the central paradox in the origin of the species , 2000, Brain Research Reviews.

[20]  A. David Callosal transfer in schizophrenia: too much or too little? , 1993, Journal of abnormal psychology.

[21]  T. Crow,et al.  Commentary on Annett, Yeo et al., Klar, Saugstad and Orr: Cerebral asymmetry, language and psychosis — the case for a Homo sapiens-specific sex-linked gene for brain growth , 1999, Schizophrenia Research.

[22]  R. M. Murray,et al.  A magnetic resonance imaging study of corpus callosum size in familial schizophrenic subjects,their relatives, and normal controls , 2000, Schizophrenia Research.

[23]  R. Reeves,et al.  Decreased Multi-Band Posterior Interhemispheric Coherence with a Lipoma on the Corpus Callosum: A Case Report of a Possible Association , 1997, Clinical EEG.

[24]  H. Markram A network of tufted layer 5 pyramidal neurons. , 1997, Cerebral cortex.

[25]  W Q Sturner,et al.  Alterations in synaptic proteins and their encoding mRNAs in prefrontal cortex in schizophrenia: a possible neurochemical basis for ‘hypofrontality’ , 1999, Molecular Psychiatry.

[26]  J. Beaumont,et al.  Brain Disconnection and Schizophrenia , 1973, British Journal of Psychiatry.

[27]  Joachim Röschke,et al.  Intra- and Interhemispheric Electroencephalogram Coherence in Siblings Discordant for Schizophrenia and Healthy Volunteers , 1997, Biological Psychiatry.

[28]  David A. Lewis,et al.  Is There a Neuropathology of Schizophrenia? Recent Findings Converge on Altered Thalamic-Prefrontal Cortical Connectivity , 2000 .

[29]  H. Brodaty,et al.  Mid-sagittal anatomy in late-onset schizophrenia , 1999, Psychological Medicine.

[30]  Reinhard Steinberg,et al.  Brain dysfunction during motor activation and corpus callosum alterations in Schizophrenia measured by cerebral blood flow and magnetic resonance imaging , 1991, Biological Psychiatry.

[31]  G. Edelman Neural Darwinism: The Theory Of Neuronal Group Selection , 1989 .

[32]  A. David,et al.  Schizophrenia and the corpus callosum: Developmental, structural and functional relationships , 1994, Behavioural Brain Research.

[33]  Mitsuru Kikuchi,et al.  Aberrant Functional Organization in Schizophrenia: Analysis of EEG Coherence during Rest and Photic Stimulation in Drug-Naive Patients , 1998, Neuropsychobiology.

[34]  G. Innocenti,et al.  Is there a genuine exuberancy of callosal projections in development? A quantitative electron microscopic study in the cat , 1983, Neuroscience Letters.

[35]  A. Toga,et al.  Mapping morphology of the corpus callosum in schizophrenia. , 2000, Cerebral cortex.

[36]  B. Pakkenberg,et al.  Pronounced reduction of total neuron number in mediodorsal thalamic nucleus and nucleus accumbens in schizophrenics. , 1990, Archives of general psychiatry.

[37]  J. S. McCasland,et al.  Cortical local circuit axons do not mature after early deafferentation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Giorgio M. Innocenti,et al.  Exuberant projection into the corpus callosum from the visual cortex of newborn cats , 1977, Neuroscience Letters.

[39]  S Marenco,et al.  The neurodevelopmental hypothesis of schizophrenia: Following a trail of evidence from cradle to grave , 2000, Development and Psychopathology.

[40]  E. Merrin,et al.  Negative symptoms and EEG alpha activity in schizophrenic patients , 1992, Schizophrenia Research.

[41]  Lynn E. DeLisi,et al.  Gender differences in corpus callosum size in first-episode schizophrenics , 1994, Biological Psychiatry.

[42]  D. Kiper,et al.  Visual stimulus-dependent changes in interhemispheric EEG coherence in ferrets. , 1999, Journal of neurophysiology.

[43]  Sifis Michelogiannis,et al.  EEG coherence during hemispheric activation in schizophrenics , 2005, European Archives of Psychiatry and Clinical Neuroscience.

[44]  Stephan Arndt,et al.  Corpus callosum shape and size in male patients with schizophrenia , 1998, Biological Psychiatry.

[45]  A. Simmons,et al.  Corpus callosum area and functioning in schizophrenic patients with auditory–verbal hallucinations , 2001, Schizophrenia Research.

[46]  S. Siris,et al.  Implications of normal brain development for the pathogenesis of schizophrenia. , 1988, Archives of general psychiatry.

[47]  David A Lewis,et al.  Intrinsic excitatory connections in the prefrontal cortex and the pathophysiology of schizophrenia , 2000, Brain Research Bulletin.

[48]  Karl J. Friston,et al.  A Voxel-Based Method for the Statistical Analysis of Gray and White Matter Density Applied to Schizophrenia , 1995, NeuroImage.

[49]  G. Innocenti,et al.  The role of pattern vision in the development ofcortico‐cortical connections , 1999, The European journal of neuroscience.

[50]  Yoshiro Okubo,et al.  EEG coherence in unmedicated schizophrenic patients: Topographical study of predominantly never medicated cases , 1992, Biological Psychiatry.

[51]  R. Murray,et al.  Meta-analysis of regional brain volumes in schizophrenia. , 2000, The American journal of psychiatry.

[52]  G M Innocenti,et al.  Growth and reshaping of axons in the establishment of visual callosal connections. , 1981, Science.

[53]  G. Wildschiødtz,et al.  Alteration of interhemisphere conduction through corpus callosum in chronic schizophrenia. , 1982, Biological psychiatry.

[54]  A. Luria The Working Brain , 1973 .

[55]  P. Williamson,et al.  Aberrant interhemispheric alpha coherence on electroencephalography in schizophrenic patients during activation tasks , 1996, Psychological Medicine.

[56]  Paul J. Harrison The neuropathology of schizophrenia , 2008 .

[57]  Y. Wada,et al.  Interhemispheric EEG Coherence in Never-Medicated Patients with Paranoid Schizophrenia: Analysis at Rest and during Photic Stimulation , 1998, Clinical EEG.

[58]  I. C. Wright,et al.  Corpus callosum size and inter-hemispheric function in schizophrenia , 1997, Schizophrenia Research.

[59]  A. Haig,et al.  An integration of 40 Hz Gamma and phasic arousal: novelty and routinization processing in schizophrenia , 2001, Clinical Neurophysiology.

[60]  David A Lewis,et al.  Catching Up on Schizophrenia Natural History and Neurobiology , 2000, Neuron.

[61]  M. L. Pucak,et al.  Peripubertal refinement of the intrinsic and associational circuitry in monkey prefrontal cortex , 1997, Neuroscience.

[62]  D. Weinberger,et al.  Evidence of dysfunction of a prefrontal-limbic network in schizophrenia: a magnetic resonance imaging and regional cerebral blood flow study of discordant monozygotic twins. , 1992, The American journal of psychiatry.

[63]  A. David Divided Visual Field Studies in Schizophrenia , 1989 .

[64]  A. David,et al.  Severe psychiatric disturbance and abnormalities of the corpus callosum: review and case series. , 1993, Journal of neurology, neurosurgery, and psychiatry.

[65]  Symms,et al.  Investigating neuropathological abnormalities in schizophrenia using magnetization transfer imaging , 2001 .

[66]  Franco Lepore,et al.  Bilateral interaction in the second somatosensory area (SII) of the cat and contribution of the corpus callosum , 1990, Brain Research.

[67]  B. Sakmann,et al.  Dendritic GABA Release Depresses Excitatory Transmission between Layer 2/3 Pyramidal and Bitufted Neurons in Rat Neocortex , 1999, Neuron.

[68]  A. Sampson,et al.  Decreased somal size of deep layer 3 pyramidal neurons in the prefrontal cortex of subjects with schizophrenia. , 2001, Archives of general psychiatry.

[69]  R. Hoffman,et al.  Schizophrenia as a disorder of developmentally reduced synaptic connectivity. , 2000, Archives of general psychiatry.

[70]  G. Innocenti,et al.  Computational Structure of Visual Callosal Axons , 1994, The European journal of neuroscience.

[71]  G M Innocenti,et al.  The development of the corpus callosum in cats: A light‐ and electron‐ microscopic study , 1988, The Journal of comparative neurology.

[72]  D. M. Parker,et al.  Developments in Clinical and Experimental Neuropsychology , 1989 .

[73]  W. Singer,et al.  Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex , 1991, Science.

[74]  U Salvolini,et al.  Role of the corpus callosum in the somatosensory activation of the ipsilateral cerebral cortex: an fMRI study of callosotomized patients , 1999, The European journal of neuroscience.

[75]  Jacqueline Spiegel-Cohen,et al.  Shape and size of the corpus callosum in schizophrenia and schizotypal personality disorder , 2000, Schizophrenia Research.

[76]  P. Bovet,et al.  Visual binding abilities in the initial and advanced stages of schizophrenia , 2001, Acta psychiatrica Scandinavica.

[77]  P. Williamson,et al.  EEG coherence and syndromes in schizophrenia , 1997, British Journal of Psychiatry.

[78]  J. Rothstein,et al.  The expression of glutamate transporter GLT-1 in the rat cerebral cortex is down-regulated by the antipsychotic drug clozapine , 2001, Molecular Psychiatry.

[79]  R. Eckhorn,et al.  Coherent oscillations: A mechanism of feature linking in the visual cortex? , 1988, Biological Cybernetics.

[80]  Cerebral Asymmetry, Language and Psychosis , 1998 .

[81]  P. Goldman-Rakic,et al.  The reduced neuropil hypothesis: a circuit based model of schizophrenia , 1999, Biological Psychiatry.

[82]  P. Munk-Jørgensen Happy New Year 2001 , 2001, Ugeskrift for laeger.

[83]  G. Innocenti Exuberant development of connections, and its possible permissive role in cortical evolution , 1995, Trends in Neurosciences.

[84]  A. Salamy,et al.  Commissural transmission: maturational changes in humans. , 1978, Science.

[85]  Fred L Bookstein,et al.  Landmark-based morphometric analysis of first-episode schizophrenia , 1999, Biological Psychiatry.

[86]  E. Callaway,et al.  Emergence and refinement of clustered horizontal connections in cat striate cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[87]  G. Spidalieri,et al.  Relevance of the callosal transfer in defining the peripheral reactivity of somesthetic cortical neurones. , 1973, Archives italiennes de biologie.

[88]  D. Heiss,et al.  Corpus callosum size in schizophrenia – a magnetic resonance imaging analysis , 1999, European Archives of Psychiatry and Clinical Neuroscience.

[89]  N. Andreasen,et al.  Hypofrontality in schizophrenia: distributed dysfunctional circuits in neuroleptic-naïve patients , 1997, The Lancet.

[90]  Peter Rappelsberger,et al.  Low frontal electroencephalographic coherence in neuroleptic-free schizophrenic patients , 1998, Biological Psychiatry.

[91]  P. Huttenlocher Synaptic density in human frontal cortex - developmental changes and effects of aging. , 1979, Brain research.

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

[93]  Schwartz Bd,et al.  A corpus callosal deficit in sequential analysis by schizophrenics. , 1984 .

[94]  D. Kiper,et al.  Visual stimulus-dependent changes in interhemispheric EEG coherence in humans. , 1999, Journal of neurophysiology.

[95]  E G Jones,et al.  Subnucleus-specific loss of neurons in medial thalamus of schizophrenics. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[96]  E. Merrin,et al.  Negative symptoms and EEG alpha in schizophrenia: a replication , 1996, Schizophrenia Research.

[97]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[98]  B. Pakkenberg,et al.  Total nerve cell number in neocortex in chronic schizophrenics and controls estimated using optical disectors , 1993, Biological Psychiatry.

[99]  P W Woodruff,et al.  Meta-analysis of corpus callosum size in schizophrenia. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[100]  P. Rakić,et al.  Axon overproduction and elimination in the corpus callosum of the developing rhesus monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[101]  W. Singer,et al.  Interhemispheric asymmetries of the modular structure in human temporal cortex. , 2000, Science.

[102]  W Singer,et al.  Role of the temporal domain for response selection and perceptual binding. , 1997, Cerebral cortex.

[103]  I. Feinberg,et al.  Schizophrenia: caused by a fault in programmed synaptic elimination during adolescence? , 1982, Journal of psychiatric research.

[104]  M. Phillips,et al.  Stroop interference and facilitation in the cerebral hemispheres in schizophrenia , 1996, Schizophrenia Research.

[105]  Friedemann Pulvermüller,et al.  Interhemispheric cooperation during word processing: evidence for callosal transfer dysfunction in schizophrenic patients , 2000, Schizophrenia Research.

[106]  Karl J. Friston,et al.  Theoretical neurobiology and schizophrenia. , 1996, British medical bulletin.

[107]  V. Mountcastle,et al.  An organizing principle for cerebral function : the unit module and the distributed system , 1978 .

[108]  H. Loos,et al.  Synaptogenesis in human visual cortex — evidence for synapse elimination during normal development , 1982, Neuroscience Letters.

[109]  L. Selemon,et al.  Regionally diverse cortical pathology in schizophrenia: clues to the etiology of the disease. , 2001, Schizophrenia bulletin.

[110]  B. Cragg,et al.  The development of synapses in the visual system of the cat , 1975, The Journal of comparative neurology.

[111]  R. Petty,et al.  Structural asymmetries of the human brain and their disturbance in schizophrenia. , 1999, Schizophrenia bulletin.

[112]  R. Lewine,et al.  Age at onset and sex differences in corpus callosum area in schizophrenia , 1999, Schizophrenia Research.

[113]  Evian Gordon,et al.  Gamma activity in schizophrenia: evidence of impaired network binding? , 2000, Clinical Neurophysiology.

[114]  M. Annett,et al.  The theory of an agnosic right shift gene in schizophrenia and autism , 1999, Schizophrenia Research.

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

[116]  M. Hasselmo,et al.  Gamma frequency-range abnormalities to auditory stimulation in schizophrenia. , 1999, Archives of general psychiatry.

[117]  P Boesiger,et al.  Schizophrenia: glutathione deficit in cerebrospinal fluid and prefrontal cortex in vivo , 2000, The European journal of neuroscience.

[118]  H. Kennedy,et al.  Transient projection from the superior temporal sulcus to area 17 in the newborn macaque monkey. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[119]  W. Honer,et al.  Synaptic and plasticity-associated proteins in anterior frontal cortex in severe mental illness , 1999, Neuroscience.

[120]  J. S. Barlow The mindful brain: B.M. Edelman and V.B. Mountcastle (MIT Press, Cambridge, Mass., 1978, 100 p., U.S. $ 10.00) , 1979 .

[121]  H. Möller,et al.  Corpus callosum and P300 in schizophrenia , 2001, Schizophrenia Research.

[122]  R. Coppola,et al.  An association between reduced interhemispheric EEG coherence in the temporal lobe and genetic risk for schizophrenia , 2001, Schizophrenia Research.

[123]  Ronald A. Yeo,et al.  The evolutionary genetic underpinnings of schizophrenia: the developmental instability model , 1999, Schizophrenia Research.

[124]  J. Olavarria The effect of visual deprivation on the number of callosal cells in the cat is less pronounced in extrastriate cortex than in the 17 18 border region , 1995, Neuroscience Letters.

[125]  B Boroojerdi,et al.  Transcallosal inhibition and motor conduction studies in patients with schizophrenia using transcranial magnetic stimulation. , 1999, The British journal of psychiatry : the journal of mental science.

[126]  Y. Zilberter,et al.  Dendritic release of glutamate suppresses synaptic inhibition of pyramidal neurons in rat neocortex , 2000, The Journal of physiology.

[127]  Hoffman Re,et al.  Neural network simulations, cortical connectivity, and schizophrenic psychosis. , 1997 .

[128]  Nancy C. Andreasen,et al.  Linking Mind and Brain in the Study of Mental Illnesses: A Project for a Scientific Psychopathology , 1997, Science.

[129]  G M Innocenti,et al.  Typology, early differentiation, and exuberant growth of a set of cortical axons , 1999, The Journal of comparative neurology.

[130]  G M Innocenti,et al.  Forms and measures of adult and developing human corpus callosum: Is there sexual dimorphism? , 1989, The Journal of comparative neurology.

[131]  T M Hyde,et al.  Psychiatric disturbances in metachromatic leukodystrophy. Insights into the neurobiology of psychosis. , 1992, Archives of neurology.

[132]  L. Glantz,et al.  Normal cellular levels of synaptophysin mRNA expression in the prefrontal cortex of subjects with schizophrenia , 2000, Biological Psychiatry.

[133]  K. Van Laere,et al.  The classical Stroop interference task as a prefrontal activation probe: a validation study using 99Tcm-ECD brain SPECT , 2001, Nuclear medicine communications.

[134]  D. Wahlsten,et al.  Sex Differences in the Human Corpus Callosum: Myth or Reality? , 1997, Neuroscience & Biobehavioral Reviews.

[135]  J. Foong,et al.  Neuropathological abnormalities of the corpus callosum in schizophrenia: a diffusion tensor imaging study , 2000, Journal of neurology, neurosurgery, and psychiatry.

[136]  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.

[137]  G M Innocenti,et al.  Maturation of visual callosal connections in visually deprived kittens: a challenging critical period , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[138]  Pat Levitt,et al.  Molecular Characterization of Schizophrenia Viewed by Microarray Analysis of Gene Expression in Prefrontal Cortex , 2000, Neuron.

[139]  S. Scarone,et al.  Anatomical characteristics of the corpus callosum and clinical correlates in schizophrenia , 1993, Schizophrenia Research.

[140]  P. Goldman-Rakic,et al.  Neuronal and glial somal size in the prefrontal cortex: a postmortem morphometric study of schizophrenia and Huntington disease. , 1998, Archives of general psychiatry.

[141]  Leslie G. Ungerleider,et al.  Connections of inferior temporal areas TE and TEO with medial temporal- lobe structures in infant and adult monkeys , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[142]  P. Meehl Schizotaxia, Schizotypy, Schizophrenia , 1962 .

[143]  R. Llinás,et al.  Human oscillatory brain activity near 40 Hz coexists with cognitive temporal binding. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[144]  S. Hirsch,et al.  Reduced dendritic spine density on cerebral cortical pyramidal neurons in schizophrenia , 1998, Journal of neurology, neurosurgery, and psychiatry.

[145]  J. Bullier,et al.  Structural basis of cortical synchronization. I. Three types of interhemispheric coupling. , 1995, Journal of neurophysiology.

[146]  E. Serafetinides,et al.  Schizophrenia, corpus callosum, and interhemispheric communication: A review , 1990, Psychiatry Research.

[147]  D. Lewis,et al.  Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. , 2000, Archives of general psychiatry.

[148]  P. Rakić,et al.  Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[149]  George Fein,et al.  EEG coherence in unmedicated schizophrenic patients , 1989, Biological Psychiatry.

[150]  G. Innocenti,et al.  The Development of Projections from Cerebral Cortex , 1991 .

[151]  Abraham Weizman,et al.  Hemispheric function in disorganized type schizophrenia: performance on the Quality Extinction Test , 2000, European Psychiatry.

[152]  E. Kunesch,et al.  Dysfunction of transcallosally mediated motor inhibition and callosal morphology in patients with schizophrenia , 2001, Acta psychiatrica Scandinavica.

[153]  W. Brooks,et al.  Neuropsychophysiological study of children at risk for schizophrenia: a preliminary report. , 1995, Journal of the American Academy of Child and Adolescent Psychiatry.

[154]  D. Kiper,et al.  Growth of Callosal Terminal Arbors in Primary Visual Areas of the Cat , 1996, The European journal of neuroscience.