Advertisement
Original Article| Volume 63, ISSUE 5, P512-518, March 01, 2008

Download started.

Ok

Diffusion Tensor Imaging of the Superior Longitudinal Fasciculus and Working Memory in Recent-Onset Schizophrenia

      Background

      Structural and functional abnormalities in frontal-parietal circuitry are thought to be associated with working memory (WM) deficits in patients with schizophrenia. This study examines whether recent-onset schizophrenia is associated with anatomical changes in the superior longitudinal fasciculus (SLF), the main frontal-parietal white matter connection, and whether the integrity of the SLF is related to WM performance.

      Methods

      We applied a novel registration approach (Tract-Based Spatial Statistics [TBSS]) to diffusion tensor imaging data to examine fractional anisotropy (FA) in the left and right SLF in 12 young adult patients with recent-onset schizophrenia and 17 matched control subjects.

      Results

      Schizophrenia patients showed lower FA values than control subjects across the entire SLF, with particular deficits on the left SLF. Fractional anisotropy values were correlated with performance on a verbal WM task in both patient and control groups in the left but not right SLF.

      Conclusions

      Recent-onset schizophrenia patients show deficits in frontal-parietal connections, key components of WM circuitry. Moreover, the integrity of this physiological connection predicted performance on a verbal WM task, indicating that this structural change may have important functional implications. These findings support the view that schizophrenia is a disorder of brain connectivity and implicate white matter changes detectable in the early phases of the illness as one source of this dysfunction.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Biological Psychiatry
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Chafee M.V.
        • Goldman-Rakic P.S.
        Inactivation of parietal and prefrontal cortex reveals interdependence of neural activity during memory-guided saccades.
        J Neurophysiol. 2000; 83: 1550-1566
        • Paulesu E.
        • Frith C.D.
        • Frackowiak R.S.
        The neural correlates of the verbal component of WM.
        Nature. 1993; 362: 342-345
        • Chafee M.V.
        • Goldman-Rakic P.S.
        Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial WM task.
        J Neurophysiol. 1998; 79: 2919-2940
        • Petrides M.
        • Pandya D.N.
        Association pathways of the prefrontal cortex and functional observations.
        in: Stuss D. Knight R.T. Principles of Frontal Lobe Function. Oxford University Press, New York2002
        • Klingberg T.
        Development of a superior frontal-intraparietal network for visuo-spatial working memory.
        Neuropsychologia. 2006; 44: 2171-2177
        • Lee J.
        • Park S.
        WM impairments in schizophrenia: A meta-analysis.
        J Abnorm Psychol. 2005; 114: 599-611
        • Silver H.
        • Feldman P.
        • Bilker W.
        • Gur R.C.
        WM deficit as a core neuropsychological dysfunction in schizophrenia.
        Am J Psychiatry. 2003; 160: 1809-1816
        • Goldman-Rakic P.S.
        WM dysfunction in schizophrenia.
        J Neuropsychiatry Clin Neurosci. 1994; 6: 348-357
        • Green M.F.
        What are the functional consequences of neurocognitive deficits in schizophrenia?.
        Am J Psychiatry. 1996; 153: 321-330
        • Mattay V.S.
        • Fera F.
        • Tessitore A.
        • Hariri A.R.
        • Berman K.F.
        • Das S.
        • et al.
        Neurophysiological correlates of age-related changes in WM capacity.
        Neurosci Lett. 2006; 392: 32-37
        • Narr K.L.
        • Bilder R.M.
        • Toga A.W.
        • Woods R.P.
        • Rex D.E.
        • Szeszko P.R.
        • et al.
        Mapping cortical thickness and gray matter concentration in first episode schizophrenia.
        Cereb Cortex. 2005; 15: 708-719
        • Whitford T.J.
        • Grieve S.M.
        • Farrow T.F.
        • Gomes L.
        • Brennan J.
        • Harris A.W.
        • et al.
        Progressive grey matter atrophy over the first 2-3 years of illness in first-episode schizophrenia: A tensor-based morphometry study.
        Neuroimage. 2006; 32: 511-519
        • Hulshoff Pol H.E.
        • Brans R.G.
        • van Haren N.E.
        • Schnack H.G.
        • Langen M.
        • Baare W.F.
        • et al.
        Gray and white matter volume abnormalities in monozygotic and same-gender dizygotic twins discordant for schizophrenia.
        Biol Psychiatry. 2004; 55: 126-130
        • Breier A.
        • Buchanan R.W.
        • Elkashef A.
        • Munson R.C.
        • Kirkpatrick B.
        • Gellad F.
        Brain morphology and schizophrenia.
        Arch Gen Psychiatry. 1992; 49: 921-926
        • Mori S.
        • Zhang J.
        Principles of diffusion tensor imaging and its applications to basic neuroscience research.
        Neuron. 2006; 51: 527-539
        • Buchsbaum M.S.
        • Tang C.Y.
        • Peled S.
        • Gudbjartsson H.
        • Lu D.
        • Hazlett E.A.
        • et al.
        MRI white matter diffusion anisotropy and PET metabolic rate in schizophrenia.
        Neuroreport. 1998; 9: 425-430
        • Federspiel A.
        • Begre S.
        • Kiefer C.
        • Schroth G.
        • Strik W.K.
        • Dierks T.
        Alterations of white matter connectivity in first episode schizophrenia.
        Neurobiol Dis. 2006; 22: 702-709
        • Hao Y.
        • Liu Z.
        • Jiang T.
        • Gong G.
        • Liu H.
        • Tan L.
        • et al.
        White matter integrity of the whole brain is disrupted in first-episode schizophrenia.
        Neuroreport. 2006; 17: 23-26
        • Kitamura H.
        • Matsuzawa H.
        • Shioiri T.
        • Someya T.
        • Kwee I.L.
        • Nakada T.
        Diffusion tensor analysis in chronic schizophrenia.
        Eur Arch Psychiatry Clin Neurosci. 2005; 255: 313-318
        • Kumra S.
        • Ashtari M.
        • McMeniman M.
        • Vogel J.
        • Augustin R.
        • Becker D.E.
        • et al.
        Reduced frontal white matter integrity in early-onset schizophrenia: A preliminary study.
        Biol Psychiatry. 2004; 55: 1138-1145
        • Lim K.O.
        • Hedehus M.
        • Moseley M.
        • de Crespigny A.
        • Sullivan E.V.
        • Pfefferbaum A.
        Compromised white matter tract integrity in schizophrenia inferred from diffusion tensor imaging.
        Arch Gen Psychiatry. 1999; 56: 367-374
        • Minami T.
        • Nobuhara K.
        • Okugawa G.
        • Takase K.
        • Yoshida T.
        • Sawada S.
        • et al.
        Diffusion tensor magnetic resonance imaging of disruption of regional white matter in schizophrenia.
        Neuropsychobiology. 2003; 47: 141-145
        • Szeszko P.R.
        • Ardekani B.A.
        • Ashtari M.
        • Kumra S.
        • Robinson D.G.
        • Sevy S.
        • et al.
        White matter abnormalities in first-episode schizophrenia or schizoaffective disorder: A diffusion tensor imaging study.
        Am J Psychiatry. 2005; 162: 602-605
        • Ardekani B.A.
        • Nierenberg J.
        • Hoptman M.J.
        • Javitt D.C.
        • Lim K.O.
        MRI study of white matter diffusion anisotropy in schizophrenia.
        Neuroreport. 2003; 14: 2025-2029
        • Foong J.
        • Symms M.R.
        • Barker G.J.
        • Maier M.
        • Miller D.H.
        • Ron M.A.
        Investigating regional white matter in schizophrenia using diffusion tensor imaging.
        Neuroreport. 2002; 13: 333-336
        • Price G.
        • Bagary M.S.
        • Cercignani M.
        • Altmann D.R.
        • Ron M.A.
        The corpus callosum in first episode schizophrenia: A diffusion tensor imaging study.
        J Neurol Neurosurg Psychiatry. 2005; 76: 585-587
        • Kanaan R.A.
        • Kim J.S.
        • Kaufmann W.E.
        • Pearlson G.D.
        • Barker G.J.
        • McGuire P.K.
        Diffusion tensor imaging in schizophrenia.
        Biol Psychiatry. 2005; 58: 921-929
        • Smith S.M.
        • Jenkinson M.
        • Johansen-Berg H.
        • Rueckert D.
        • Nichols T.E.
        • Mackay C.E.
        • et al.
        Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data.
        Neuroimage. 2006; 31: 1487-1505
        • Spitzer R.
        • Endicott J.
        • Williams J.
        Research diagnostic criteria.
        Arch Gen Psychiatry. 1979; 36: 29-50
        • Sternberg S.
        High-speed scanning in human memory.
        Science. 1966; 153: 652-654
        • Smith S.M.
        • Jenkinson M.
        • Woolrich M.W.
        • Beckmann C.F.
        • Behrens T.E.
        • Johansen-Berg H.
        • et al.
        Advances in functional and structural MR image analysis and implementation as FSL.
        Neuroimage. 2004; 23: S208-S219
        • Mori S.
        • Wakana S.
        • Nagae-Poetscher L.M.
        • van Zijl P.C.
        MRI Atlas of Human White Matter.
        Elsevier, Amsterdam2005
        • Stata
        Intercooled Stata 8.1 for Macintosh.
        Stata Corporation, College Station, TX2003
        • Jones D.K.
        • Symms M.R.
        • Cercignani M.
        • Howard R.J.
        The effect of filter size on VBM analyses of DT-MRI data.
        Neuroimage. 2005; 26: 546-554
        • Moreno D.
        • Burdalo M.
        • Reig S.
        • Parellada M.
        • Zabala A.
        • Desco M.
        • et al.
        Structural neuroimaging in adolescents with a first psychotic episode.
        J Am Acad Child Adolesc Psychiatry. 2005; 44: 1151-1157
        • Begre S.
        • Federspiel A.
        • Kiefer C.
        • Schroth G.
        • Dierks T.
        • Strik W.K.
        Reduced hippocampal anisotropy related to anteriorization of alpha EEG in schizophrenia.
        Neuroreport. 2003; 14: 739-742
        • Nestor P.G.
        • Kubicki M.
        • Gurrera R.J.
        • Niznikiewicz M.
        • Frumin M.
        • McCarley R.W.
        • Shenton M.E.
        Neuropsychological correlates of diffusion tensor imaging in schizophrenia.
        Neuropsychology. 2004; 18: 629-637
        • Kubicki M.
        • Westin C.
        • Maier S.
        • Frumin M.
        • Nestor P.G.
        • Salisbury D.
        • et al.
        Uncinate fasciculus findings in schizophrenia: A magnetic resonance diffusion tensor imaging study.
        Am J Psychiatry. 2002; 159: 813-820
        • Nakamura M.
        • McCarley R.W.
        • Kubicki M.
        • Dickey C.C.
        • Niznikiewicz M.A.
        • Voglmaier M.M.
        • et al.
        Fronto-temporal disconnectivity in schizotypal personality disorder: A diffusion tensor imaging study.
        Biol Psychiatry. 2005; 58: 468-478
        • Hori H.
        • Noguchi H.
        • Hashimoto R.
        • Nakabayashi T.
        • Omori M.
        • Takahashi S.
        • et al.
        Antipsychotic medication and cognitive function in schizophrenia.
        Schizophr Res. 2006; 86: 138-146