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Sensory Information Processing in Neuroleptic-Naive First-Episode Schizophrenic Patients a Functional Magnetic Resonance Imaging Study

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Sensory Information Processing in Neuroleptic-Naive First-Episode Schizophrenic Patients a Functional Magnetic Resonance Imaging Study ORIGINAL ARTICLE Sensory Information Processing in Neuroleptic-Naive First-Episode Schizophrenic Patients A Functional Magnetic Resonance Imaging Study Dieter F. Braus, MD; Wolfgang Weber-Fahr, PhD; Heike Tost, MSc; Matthias Ruf, MSc; Fritz A. Henn, PhD, MD Background: Schizophrenic disorders are thought to prefrontal cortex, and the parietal lobe (restricted to the involve widespread abnormalities in information pro- dorsal visual pathway) bilaterally. There were no no- cessing. The present study used functional magnetic reso- table differences in the primary visual cortex or the object- nance imaging and a simple and robust paradigm that specific occipitotemporal pathway. In addition, patients involved auditory and visual activation to examine ba- presented with a reduced signal change to auditory stimu- sic sensory input circuits. Our aim was to determine which lation in the left acoustic cortex. stages of the input processing network are disturbed in first-episode schizophrenic patients. Conclusions: The present study supports the concept of widespread cortical and subcortical deficits in schizo- Methods: Twelve neuroleptic-naive inpatients (para- phrenia. Our findings suggest abnormal functioning early noid subtype) were compared with 11 healthy subjects in the information processing and in high-order associa- by means of echo-planar functional magnetic resonance tion cortices already at illness onset, before the admin- imaging. In a block design, the paradigm included the istration of medication or the most confounding effects simultaneous presentation of a moving 6-Hz checker- of illness duration. The main regions have been impli- board and auditory stimuli in the form of drumbeats. The cated in visual motion perception and discrimination as subjects were asked to simply look and listen. well as in attention to sensorial events and perceptual syn- thesis. Results: In comparison with control subjects, patients showed reduced activation in the right thalamus, the right Arch Gen Psychiatry. 2002;59:696-701 HE SCHIZOPHRENIA spec- the present study was designed with the use trum is widely recognized of a simple and robust input paradigm re- as a heterogeneous disor- quiring little cognitive effort, which would der. Investigators have con- allow an evaluation of elementary informa- sistently tried to identify the tion processing. The paradigm chosen in- Tneurobiological substrate of information cluded the simultaneous presentation of 2 processing deficits that are characteristic sensory stimuli without information con- of most schizophrenic patients.1-3 It has tent, (1) an alternating visual checker- been hypothesized that there are wide- board (6 Hz) as well as (2) an acoustic spread abnormalities in the early stages of stimulus consisting of drumbeats. The use information processing leading to a cas- of 2 different modalities should involve both cade of “downstream” effects on higher the information flow through the thala- cortical functions, such as sustained at- mus to the low- and high-order sensory cor- tention, working memory, concept for- tices (V1-V5 and A1, A2) in the temporal mation, or social functioning.4 and occipital lobes and processing in the The goal of the present study was to frontoparietal cortices. Two inputs were use functional magnetic resonance (fMR) chosen to stimulate perceptual synthesis and imaging5 to demonstrate abnormality in in- to maximize activation of the heteromodal formation processing circuits in first- association cortices. Thus far, the func- episode, neuroleptic-naive schizophrenic tional interaction of the information pro- patients. In general, functional imaging find- cessing stream via visual and acoustic in- From the Central Institute ings in acutely ill schizophrenic patients put channels has not been directly studied of Mental Health (ZI), have been criticized, as patients might be in schizophrenia. Therefore, this study may NMR-Research, Mannheim, unable to understand and perform compli- serve as a starting point for further re- Germany. cated cognitive tasks. Keeping this in mind, search aimed at identifying functional dif- (REPRINTED) ARCH GEN PSYCHIATRY/ VOL 59, AUG 2002 WWW.ARCHGENPSYCHIATRY.COM 696 ©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/30/2021 SUBJECTS AND METHODS had been explained to all participants. The study was ap- proved by the local university ethics committee. SUBJECTS PROCEDURE Twelve inpatients (6 men and 6 women; average [±SD] age, The fMR imaging paradigm included the simultaneous pre- 25.1±4.8 years; school education, 10.6±1.8 years) living sentation of a flickering 6-Hz checkerboard and auditory in the community of Mannheim, Germany, and satisfying stimuli in the form of drumbeats, with the specific instruc- DSM-IV as well as International Classification of Diseases, tion just to look and listen. Visual stimuli were generated 10th Revision (ICD-10) criteria for schizophrenia along with by a computer (Apple PowerBook; Apple Computer Corp, 11 healthy control subjects (6 men and 5 women; average Cupertino, Calif; MacStim; David Darby, PhD, FRACP, West age, 29.4±6.2 years; school education, 12.0±1.4 years) par- Melbourne, Australia) and displayed on a back projection ticipated in this study. Control subjects were recruited plane at the foot end of the scanner via a liquid crystal dis- through advertisements; all patients entered the study af- play projector (Sharp Electronics Corporation, Mahway, ter first psychiatric hospitalization. All were right-handed NJ). Subjects were in a supine position and viewed the screen according to the Edinburgh Handedness Inventory.6 All in- through an adjustable mirror fixed to the head coil. Acous- patients were neuroleptic-naive, having their first schizo- tic stimuli were presented through customized magnetic phrenic episode with the predominance of delusions, hal- resonance headphones. The 2 experimental conditions lucinations, and distrust. Particular care was taken to exclude (stimulation and fixation) were recorded in 5 sequences patients with a history of neurologic disorders or sub- of 10 measurements in alternating order. stance abuse. All patients had undergone thorough neu- rologic examination, showing no abnormalities. Urine IMAGE ACQUISITION screening for drug usage was negative. All stabilized patients were rediagnosed 6 months after the initial exami- Images were acquired on a standard clinical 1.5-T MR im- nation, and the diagnosis was stable in all cases. ager (Siemens AG, Munich, Germany). For fMR imaging, a The healthy volunteers were given a structured screen- standard echo planar imaging sequence (repetition time, 1.8 ing interview. Exclusion criteria included a history of milliseconds; echo time, 66 milliseconds; ␣=90°;T2* con- significant medical, neurologic, or psychiatric illnesses as trast) with an in-plane resolution of 64ϫ64 pixels (19 slices; well as substance abuse. Written informed consent was ob- tained after the purpose of the study and the procedures Continued on next page ferences in the various levels of information processing defi- dorsolateral thalamic areas corresponding to the lateral cits. We hypothesized that even minimal cognitive effort and medial geniculate nuclei. Increased activation was might disclose dysfunction in different levels of the infor- also seen in the dorsolateral prefrontal cortex, where a mation processing network, particularly in the thalamus pronounced right-sided activation in the inferior por- and frontoparietal association areas. tion was detected. Figure 1 shows the localization of the activation overlaid onto a glass brain. RESULTS GROUP ANALYSIS OF FIRST-EPISODE The study groups did not differ significantly with respect SCHIZOPHRENIC PATIENTS to age, sex, or educational achievement. On average, pa- tients were investigated 6.5 months after inception of pro- The group analysis of the different perceptual conditions dromal signs. Patients presented with moderate psychotic in the neuroleptic-naive first-episode patient group showed symptoms as indicated by the Brief Psychiatric Rating Scale a significant activation in the primary visual (V1), ex- (mean±SD score, 49.9±5.7). None of the participants had trastriate (V2-V5), and auditory cortices (A1, A2) of the ever received neuroleptic medication before being en- brain. Thalamic activation patterns were more pro- rolled in the study. Overall head motions were evaluated nounced in the lateral and medial geniculate nuclei of the with SPM99 software. Two patients and 1 control subject left hemisphere. A significant blood oxygen level– had to be excluded because of motion artifacts exceeding dependent response of prefrontal areas was totally miss- 1.5 mm in the x, y, or z direction. Structural MR images ing in our patient group. Table 1 shows the amount and and showed no abnormalities in any of the participants. the localization of stimulus-induced activations. GROUP ANALYSIS OF HEALTHY SUBJECTS INTERACTION ANALYSIS Comparing visual and acoustic stimulation and fixa- The application of a rigorous interaction analysis allows the tion, the group analysis showed a significant (PϽ.05) ac- selective detection of cerebral areas that are less active in tivation of the primary visual cortex (V1) and extrastri- the schizophrenic sample and enhanced in healthy con- ate areas (V2-V5) as well as the superior temporal auditory trol subjects. The schizophrenic patients showed a mark- cortices A1 and A2 (Table 1). A stimulation-induced edly reduced response
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