Impaired target detection in schizophrenia and the ventral attentional network: Findings from a joint event-related potential-functional MRI analysis
Jonathan K Wynn, Amy M Jimenez, Brian J Roach, Alexander Korb, Junghee Lee, William P Horan, Judith M Ford, Michael F Green, Jonathan K Wynn, Amy M Jimenez, Brian J Roach, Alexander Korb, Junghee Lee, William P Horan, Judith M Ford, Michael F Green
Abstract
Schizophrenia patients have abnormal neural responses to salient, infrequent events. We integrated event-related potentials (ERP) and fMRI to examine the contributions of the ventral (salience) and dorsal (sustained) attention networks to this dysfunctional neural activation. Twenty-one schizophrenia patients and 22 healthy controls were assessed in separate sessions with ERP and fMRI during a visual oddball task. Visual P100, N100, and P300 ERP waveforms and fMRI activation were assessed. A joint independent components analysis (jICA) on the ERP and fMRI data were conducted. Patients exhibited reduced P300, but not P100 or N100, amplitudes to targets and reduced fMRI neural activation in both dorsal and ventral attentional networks compared with controls. However, the jICA revealed that the P300 was linked specifically to activation in the ventral (salience) network, including anterior cingulate, anterior insula, and temporal parietal junction, with patients exhibiting significantly lower activation. The P100 and N100 were linked to activation in the dorsal (sustained) network, with no group differences in level of activation. This joint analysis approach revealed the nature of target detection deficits that were not discernable by either imaging methodology alone, highlighting the utility of a multimodal fMRI and ERP approach to understand attentional network deficits in schizophrenia.
Keywords: ERP; Joint ICA; Oddball; Salience network; fMRI.
Figures
References
- Andreasen N.C., Pressler M., Nopoulos P., Miller D., Ho B.C. Antipsychotic dose equivalents and dose-years: a standardized method for comparing exposure to different drugs. Biol. Psychiatry. 2010;67(3):255–262.
- Beckmann C.F., Jenkinson M., Smith S.M. General multilevel linear modeling for group analysis in fMRI. Neuroimage. 2003;20(2):1052–1063.
- Bledowski C., Prvulovic D., Hoechstetter K., Scherg M., Wibral M., Goebel R., Linden D.E. Localizing P300 generators in visual target and distractor processing: a combined event-related potential and functional magnetic resonance imaging study. J. Neurosci. 2004;24(42):9353–9360.
- Bramon E., Rabe-Hesketh S., Sham P., Murray R.M., Frangou S. Meta-analysis of the P300 and P50 waveforms in schizophrenia. Schizophr. Res. 2004;70(2–3):315–329.
- Calhoun V.D., Adali T., Pearlson G.D., Kiehl K.A. Neuronal chronometry of target detection: fusion of hemodynamic and event-related potential data. Neuroimage. 2006;30(2):544–553.
- Calhoun V.D., Wu L., Kiehl K., Eichele T., Pearlson G. Aberrant processing of deviant stimuli in schizophrenia revealed by fusion of FMRI and EEG data. Acta Neuropsych. 2010;22(3):127–138.
- Clementz B.A., Wang J., Keil A. Normal electrocortical facilitation but abnormal target identification during visual sustained attention in schizophrenia. J. Neurosci. 2008;28(50):13411–13418.
- Corbetta M., Shulman G.L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 2002;3(3):201–215.
- Cornblatt B.A., Erlenmeyer-Kimling L. Global attentional deviance as a marker of risk for schizophrenia: specificity and predictive validity. J. Abnorm. Psychol. 1985;94(4):470–486.
- Donchin E., Coles M.G.H. Is the P300 component a manifestation of context updating? Behav. Brain Sci. 1988;11(03):357–427.
- Downar J., Crawley A.P., Mikulis D.J., Davis K.D. A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. J. Neurophysiol. 2002;87(1):615–620.
- First M.B., Gibbons M., Spitzer R.L., Williams J.B.W. Biometrics Research Department; New York: 1996. Structured Clinical Interview for DSM-IV Axis II Personality Disorders.
- First M.B., Gibbons M., Spitzer R.L., Williams J.B.W. Biometrics Research Department; New York: 1996. Users Guide for the Structured Clinical Interview for DSM-IV Axis I Disorders-Research Version (SCID-1, Version 2.0, February 1996 Final Version)
- Ford J.M. Schizophrenia: the broken P300 and beyond. Psychophysiology. 1999;36(6):667–682.
- Ford J.M., Roach B.J., Miller R.M., Duncan C.C., Hoffman R.E., Mathalon D.H. When it's time for a change: failures to track context in schizophrenia. Int. J. Psychophysiol. 2010;78(1):3–13.
- Ford J.M., White P., Lim K.O., Pfefferbaum A. Schizophrenics have fewer and smaller P300s: a single-trial analysis. Biol. Psychiatry. 1994;35(2):96–103.
- Foxe J.J., Doniger G.M., Javitt D.C. Early visual processing deficits in schizophrenia: impaired P1 generation revealed by high-density electrical mapping. Neuroreport. 2001;12(17):3815–3820.
- Gur R.E., Turetsky B.I., Loughead J., Snyder W., Kohler C., Elliott M., Pratiwadi R., Ragland J.D., Bilker W.B., Siegel S.J., Kanes S.J., Arnold S.E., Gur R.C. Visual attention circuitry in schizophrenia investigated with oddball event-related functional magnetic resonance imaging. Am. J. Psychiatry. 2007;164(3):442–449.
- Guthrie D., Buchwald J.S. Significance testing of difference potentials. Psychophysiology. 1991;28(2):240–244.
- Harsay H.A., Spaan M., Wijnen J.G., Ridderinkhof K.R. Error awareness and salience processing in the oddball task: shared neural mechanisms. Front. Hum. Neurosci. 2012;6:246.
- Herrmann C.S., Knight R.T. Mechanisms of human attention: event-related potentials and oscillations. Neurosci. Biobehav. Rev. 2001;25(6):465–476.
- Jardri R., Pouchet A., Pins D., Thomas P. Cortical activations during auditory verbal hallucinations in schizophrenia: a coordinate-based meta-analysis. Am. J. Psychiatry. 2011;168(1):73–81.
- Jeon Y.W., Polich J. Meta-analysis of P300 and schizophrenia: patients, paradigms, and practical implications. Psychophysiology. 2003;40(5):684–701.
- Kiehl K.A., Laurens K.R., Duty T.L., Forster B.B., Liddle P.F. Neural sources involved in auditory target detection and novelty processing: an event-related fMRI study. Psychophysiology. 2001;38(1):133–142.
- Kiehl K.A., Stevens M.C., Celone K., Kurtz M., Krystal J.H. Abnormal hemodynamics in schizophrenia during an auditory oddball task. Biol. Psychiatry. 2005;57(9):1029–1040.
- Kim D.I., Mathalon D.H., Ford J.M., Mannell M., Turner J.A., Brown G.G., Belger A., Gollub R., Lauriello J., Wible C., O'Leary D., Lim K., Toga A., Potkin S.G., Birn F., Calhoun V.D. Auditory oddball deficits in schizophrenia: an independent component analysis of the fMRI multisite function BIRN study. Schizophr. Bull. 2009;35(1):67–81.
- Kim H. Involvement of the dorsal and ventral attention networks in oddball stimulus processing: A meta-analysis. Hum. Brain Mapp. 2014;35(5):2265–2284.
- Kiss I., Dashieff R.M., Lordeon P. A parieto-occipital generator for P300: evidence from human intracranial recordings. Int. J. Neurosci. 1989;49(1–2):133–139.
- Kopelowicz A., Ventura J., Liberman R.P., Mintz J. Consistency of brief psychiatric rating scale factor structure across a broad spectrum of schizophrenia patients. Psychopathology. 2008;41(2):77–84.
- Kucyi A., Hodaie M., Davis K.D. Lateralization in intrinsic functional connectivity of the temporoparietal junction with salience- and attention-related brain networks. J. Neurophysiol. 2012;108(12):3382–3392.
- MacDonald A.W., III Building a clinically relevant cognitive task: case study of the AX paradigm. Schizophr. Bull. 2008;34(4):619–628.
- Machado S., Arias-Carrión O., Sampaio I., Bittencourt J., Velasques B., Teixeira S., Nardi A.E., Piedade R., Ribeiro P. Source imaging of P300 visual evoked potentials and cognitive functions in healthy subjects. Clin. E.E.G. Neurosci. 2014:1–7.
- Martínez A., Hillyard S.A., Bickel S., Dias E.C., Butler P.D., Javitt D.C. Consequences of magnocellular dysfunction on processing attended information in schizophrenia. Cereb. Cortex. 2012;22(6):1282–1293.
- Mathalon D.H., Hoffman R.E., Watson T.D., Miller R.M., Roach B.J., Ford J.M. Neurophysiological distinction between schizophrenia and schizoaffective disorder. Front. Hum. Neurosci. 2010;3:70.
- McCarthy G., Wood C.C. Intracranial recordings of endogenous ERPs in humans. Electroencephalogr. Clin. Neurophysiol. 1987;39:331–337.
- Molholm S., Ritter W., Murray M.M., Javitt D.C., Schroeder C.E., Foxe J.J. Multisensory auditory–visual interactions during early sensory processing in humans: A high-density electrical mapping study. Cogn. Brain Res. 2002;14(1):115–128.
- Mulert C., Jäger L., Schmitt R., Bussfeld P., Pogarell O., Möller H.J., Juckel G., Hegerl U. Integration of fMRI and simultaneous EEG: towards a comprehensive understanding of localization and time-course of brain activity in target detection. Neuroimage. 2004;22(1):83–94.
- Nuechterlein K.H., Dawson M.E. Information processing and attentional functioning in the developmental course of schizophrenic disorders. Schizophrenia Bulletin. 1984;10(2):160–203.
- Palaniyappan L., Liddle P.F. Does the salience network play a cardinal role in psychosis? An emerging hypothesis of insular dysfunction. J. Psychiatry Neurosci. 2012;37(1):17–27.
- Palaniyappan L., Mallikarjun P., Joseph V., White T.P., Liddle P.F. Reality distortion is related to the structure of the salience network in schizophrenia. Psychol. Med. 2011;41(8):1701–1708.
- Polich J. P300 from a passive auditory paradigm. Electroencephalogr. Clin. Neurophysiol. 1989;74(4):312–320.
- Schechter I., Butler P.D., Zemon V.M., Revheim N., Saperstein A.M., Jalbrzikowski M., Pasternak R., Silipo G., Javitt D.C. Impairments in generation of early-stage transient visual evoked potentials to magno- and parvocellular-selective stimuli in schizophrenia. Clin. Neurophysiol. 2005;116(9):2204–2215.
- Seeley W.W., Menon V., Schatzberg A.F., Keller J., Glover G.H., Kenna H., Reiss A.L., Greicius M.D. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 2007;27(9):2349–2356.
- Silverstein S.M., Berten S., Essex B., All S.D., Kasi R., Little D.M. Perceptual organization and visual search processes during target detection task performance in schizophrenia, as revealed by fMRI. Neuropsychologia. 2010;48(10):2886–2893.
- Slotnick S.D., Moo L.R., Segal J.B., Hart J. Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. Cogn. Brain Res. 2003;17(1):75–82.
- Sponheim S.R., McGuire K.A., Stanwyck J.J. Neural anomalies during sustained attention in first-degree biological relatives of schizophrenia patients. Biol. Psychiatry. 2006;60(3):242–252.
- Sutton S., Tueting P., Zubin J., John E.R. Information delivery and the sensory evoked potential. Science. 1967;155(3768):1436–1439.
- Woolrich M. Robust group analysis using outlier inference. Neuroimage. 2008;41(2):286–301.
- Ventura J., Nuechterlein K.I., Subotnik K., Gilbert E. 1995. Symptom Dimensions in Recent-onset Schizophrenia: The 24-Item Expanded BPRS.
- Woolrich M.W., Behrens T.E., Beckmann C.F., Jenkinson M., Smith S.M. Multilevel linear modelling for FMRI group analysis using Bayesian inference. Neuroimage. 2004;21(4):1732–1747.
Source: PubMed