Early sensory–perceptual processing deficits for affectively valenced inputs are more pronounced in schizophrenia patients with a history of violence than in their non-violent peers

doi:10.1093/scan/nss052 SCAN (2013) 8, 678 ^ 687 Early sensory–perceptual processing deficits for affectively valenced inputs are more pronounced in schizophrenia patients with a history of violence than in their non-violent peers Pierfilippo De Sanctis,1,2 John J. Foxe,1,2 Pal Czobor,1,3 Glenn R. Wylie,4 Stephanie M. Kamiel,1 Jessica Huening,1 Mike Nair-Collins,1 and Menahem I. Krakowski1 1 The Cognitive Neurophysiology Laboratory, The Nathan S. Kline Institute for Psychiatric Research, Orangeburg, NY 10962, 2The Sheryl and Daniel R. Tishman Cognitive Neurophysiology Laboratory, Children’s Evaluation and Rehabilitation Center (CERC), Department of Pediatrics and Neuroscience, Albert Einstein College of Medicine, Bronx, NY 10461, USA, 3Department of Psychiatry and Psychotherapy, Semmelweis University, Budapest, Hungary and 4Neuropsychology and Neuroscience Laboratory, Kessler Foundation Research Center, NJ 07052, USA Keywords: Schizophrenia; violence; amygdala; emotion; event-related potential INTRODUCTION Violent behavior in patients with schizophrenia, while relatively uncommon, has prevalence rates ranging from 15.3% to 19.1% (Swanson et al., 2004, 2006). The presence of these behaviors is a significant public health issue in that they often result in prolonged hospitalization, can greatly interfere with reintegration into the community and are associated with higher rates of criminal conviction (Hodgins et al., 2005). Understanding the underlying neurobiology that predisposes a subset of patients to violent behaviors is therefore of primary importance. Multiple risk factors of a clinical, interpersonal and social–environmental nature have been identified (Swanson et al., 2004, 2006; Fazel et al., 2009a, b). It should be noted, however, that patients with schizophrenia show significant deficits in basic affective processing (Kayton and Koh, 1975), and that such deficits have been identified as an important precursor to violence in the general population (Davidson et al., 2000). We focus here on disturbances in the processing of affectively valenced inputs in patients with schizophrenia and their potential relationship to violent behaviors in this population. Received 30 October 2011; Accepted 18 April 2012 Advance Access publication 3 May 2012 Sincere thanks go to Eileen Zenz and Melissa Brady for help with recruitment, clinical interviewing and neuropsychological testing, Karen Nolan (PhD) and Constance Shope (PhD) for clinical interviewing and Emma Jane Forde, Ryan Bell, Kristen Morie for EEG data collection. Dr Krakowski takes full responsibility for the integrity of the data and attests that all authors had full access to all the data in this study. Primary support for this work was provided by an RO1 grant from the U.S. National Institute of Mental Health (MH74767). Additional support was derived from MH85322. Correspondence should be addressed to Pierfilippo De Sanctis. The Cognitive Neurophysiology Laboratory, Departments of Pediatrics and Neuroscience, Albert Einstein College of Medicine, Van Etten Building – 1C, 1225 Morris Park Avenue, Bronx, NY 10461, USA. E-mail: Disturbances in the processing of affective information in patients with schizophrenia include impaired recognition of facial affect (Morris et al., 2009; Leitman et al., 2010), and deficits in their abilities to interpret the emotional prosodic content of speech (Ross et al., 2001; Leitman et al., 2005, 2007). One consistent finding is a negativity bias, whereby patients show a strong inclination to misidentify neutral stimuli as negatively valenced (Edwards et al., 2001; Kohler et al., 2003; Premkumar et al., 2008; Tsoi et al., 2008). Such inabilities to accurately identify emotional valence, accompanied by a bias to interpret situations in a negative light, could heighten the risk of violence in schizophrenia. To our knowledge, possible links between affective deficits and violent behaviors has yet to be investigated in schizophrenia. Using high-density neurophysiological recordings, we tested how early during the processing of emotionally valenced stimuli, evidence of aberrant processing would be observed in patients relative to healthy controls, and in turn, whether more severe deficits would be evident in patients with a history of violent behaviors. Event-related potentials (ERPs) provide temporally precise measures of information processing well suited to probe for modulation in response to affectively valenced inputs, allowing for the dissociation of early sensory–perceptual from later higher order cognitive processing stages. Studies in healthy populations have reported modulation of very early (60–90 ms) and later (500–800 ms) ERP components, pointing to valence sensitivity during both processing stages. Direct recordings from the amygdala in humans have shown fear-specific modulations as early as 140 ms after stimulation (Krolak-Salmon et al., 2004; Pourtois et al., 2010). Scalp-recorded valence-related ERP modulations have been reported at just 90 ms (Pourtois et al., 2004). In a clever experiment, pairings of facial stimuli were presented, ß The Author (2012). Published by Oxford University Press. For Permissions, please email: Individuals with schizophrenia are more prone to violent behaviors than the general population. It is increasingly recognized that processing of emotionally valenced stimuli is impaired in schizophrenia, a deficit that may play a role in aggressive behavior. Our goal was to establish whether patients with a history of violence would show more severe deficits in processing emotionally valenced inputs than non-violent patients. Using event-related potentials, we measured how early during processing of emotional valence, evidence of aberrant function was observed. A total of 42 schizophrenia patients (21 with history of violence; 21 without) and 28 healthy controls were tested. Participants performed an inhibitory control task, making speeded responses to pictorial stimuli. Pictures occasionally repeated twice and participants withheld responses to these repeats. Valenced pictures from the International Affective Picture System were presented. Results in controls showed modulations during the earliest phases of sensory processing (<100 ms) for negatively valenced pictures. A cascade of modulations ensued, involving sensory and perceptual processing stages. In contrast, neither schizophrenia group showed early differentiation. Non-violent patients showed earliest modulations beginning 150 ms. For violent patients, however, earliest modulations were further delayed and highly attenuated. The current study reveals sensory–perceptual processing dysfunction for negatively valenced inputs, which is particularly pronounced in aggressive patients. Violent schizophrenia and affective processing dysfunction MATERIALS AND METHODS Participants A total of 21 patients with a history of violence (VS), 21 without a history of violence (NVS) and 28 healthy cont (...truncated)