Sensory gating in adult with attention-deficit/hyperactivity disorder: Event-evoked potential and perceptual experience reports comparisons with schizophrenia
Introduction
Attention-deficit/hyperactivity disorder (ADHD) is one of the most prevalent psychiatric disorders; the estimated prevalence ranges from 3% to 5% in adults (Caci, Morin, & Tran, 2014Fayyad et al., 2007, Hudziak et al., 2005). Inattention, hyperactivity and impulsivity are the core symptoms of ADHD (American Psychiatric Association, 2000). Inattention may be related to an inability to control sensitivity to sensory stimuli (Venables, 1964). Patients with ADHD report being flooded with sensory stimuli; therefore, attention and information processing may be deficient in ADHD (Biederman, 2005, Faraone et al., 2000). The attention of patients with ADHD may be involuntarily drowned by many irrelevant environmental stimuli leading to impaired attention on relevant stimuli (Olincy et al., 2000). This hypothesis can be related to a sensory gating deficit. Sensory gating is the ability to filter intrusive sensory information, which is a specific and elementary form of pre-attentive information processing (Braff & Geyer, 1990). Sensory gating may protect higher cognitive function from flooding by irrelevant sensory information (Venables, 1964). Sensory gating has been largely investigated in schizophrenia (Micoulaud Franchi, Vion Dury, & Cermolacce, 2013) but very few investigated in ADHD.
A sensory gating deficit can be assessed with auditory event-related potentials (ERP) (Freedman et al., 1987) and with a self-report questionnaire (the Sensory Gating Inventory, SGI) (Hetrick, Erickson, & Smith, 2012). Auditory ERP measure the suppression of the P50 component (a middle latency positive ERP component occurring approximately 50 ms after the onset of a brief auditory stimulus) in a dual-click conditioning-testing paradigm (Freedman et al., 1987). P50 suppression refers to the decrement of the P50 amplitude after the second stimulus (testing stimulus, S2) versus the P50 amplitude after the first stimulus (conditioning stimulus, S1) (Adler et al., 1982). The decrement of the P50 amplitude is considered as a neurophysiological measure of the ability to filter intrusive sensory information (Light & Braff, 2003). The SGI is composed of 36 items addressing a broad range of subjective daily perceptual experiences related to sensory gating. The psychometric properties of the SGI indicate that it provides valuable information on four dimensions of perceptual anomalies: Perceptual Modulation (PM; linked to 16 items, e.g., “My hearing is so sensitive that ordinary sounds become uncomfortable”), Over-Inclusion (OI; 7 items, e.g., “I notice background noises more than other people”), Distractibility (D; 8 items, e.g., “There are times when I can’t concentrate with even the slightest sounds going on”), and Fatigue–Stress Modulation (FS; 5 items, e.g., “It seems that sounds are more intense when I’m stressed”) (Hetrick et al., 2012, Micoulaud-Franchi et al., 2014b).
Many studies on schizophrenia have identified a P50 suppression deficit (Adler et al., 1982, Clementz et al., 1997). Patients with schizophrenia scored higher than healthy subjects did on the SGI and report being flooded with sensory stimuli (Micoulaud-Franchi et al., 2014a). In addition, patients with high P50 suppression deficits report the most perceptual abnormal experiences (Micoulaud-Franchi et al., 2014a). These data confirm an inability to control the sensitivity to sensory stimuli in schizophrenia (McGhie & Chapman, 1961; Venables, 1964). Thus, a sensory gating deficit can be considered a core psychophysiological deficit in schizophrenia (de Wilde, Bour, Dingemans, Koelman, & Linszen, 2007), with a relationship between abnormal neurophysiological (ERP) and clinical (SGI) features of sensory gating (Micoulaud-Franchi et al., 2014a).
Few studies investigated sensory gating deficit in adults with ADHD. Only two studies investigated P50 suppression (Holstein et al., 2013, Olincy et al., 2000). Olincy et al. (2000) were the first to investigate P50 suppression in adults with ADHD compared to healthy subjects and reported no significant differences. The authors suggested that the lack of significance may have be due to the small sample size of the their study (16 adults with ADHD) (Olincy et al., 2000). Holstein et al. (2013) investigated P50 suppression in 26 adults with ADHD and reported a significant P50 suppression deficit compared to healthy subjects. The same result was found in 22 children and adolescents with ADHD (Durukan et al., 2011). These contradictory studies highlight the need for further investigations of P50 suppression in adults with ADHD. Only one study investigated the abnormal perceptual experience of being flooded with sensory stimuli in adults with ADHD (Sable et al., 2012). Using a short version of the SGI (17 items), Sable et al. (2012) confirmed that adults with ADHD (22 subjects) reported higher scores in the SGI than healthy subjects, particularly on the Distractibility dimension. However, the short version of the SGI did not investigate the Fatigue–Stress Modulation dimension that could be important in ADHD because of the role of fatigue (Yoon, Jain, & Shapiro, 2013), stress (Purper-Ouakil, Wohl, Michel, Mouren, & Gorwood, 2004) and vigilance alterations (Hegerl & Hensch, 2014; Philip et al., 2005). Finally, to the best of our knowledge, no study investigated both P50 suppression and abnormal perceptual experiences with all 36 items of the SGI in adults with ADHD, as has been performed with patients with schizophrenia (Micoulaud-Franchi et al., 2014a). Thus, the relationships between abnormal neurophysiological (ERP) and clinical (SGI) features of sensory gating need to be investigated in adults with ADHD.
Therefore, the aim of the present study was to investigate both P50 suppression and SGI scores in adults with ADHD compared to patients with schizophrenia and healthy subjects to get a better understanding of sensory gating deficit in adults with ADHD (Johannesen et al., 2008, Kisley et al., 2004). The primary hypotheses were that adults with ADHD in comparison with healthy subjects: (i) would exhibit P50 suppression deficit (Holstein et al., 2013) and (ii) would report higher overall SGI scores (Sable et al., 2012). The secondary hypotheses were that adults with ADHD in comparison with patients with schizophrenia: (i) would report more abnormal perceptual experiences on the Distractibility dimension (Sable et al., 2012) and the Fatigue–Stress dimension of the SGI, in line with the core inattention symptom in ADHD (American Psychiatric Association, 2000) and the role of fatigue and stress in this disorder (Purper-Ouakil et al., 2004, Yoon et al., 2013), and (ii) would exhibit the same relationship found between P50 suppression deficit and SGI scores (Micoulaud-Franchi et al., 2014a).
Section snippets
Participants
Twenty-four adult patients with ADHD (30.2 ± 7.9 years, female: 8) were recruited from the Department of Psychiatry, Marseille University Hospital, France. Comparison subjects were 24 outpatients with chronic and clinically stable schizophrenia (31.3 ± 10.8 years, female: 8) and 24 healthy subjects (36.5 ± 11.2 years, female: 8). Patients with ADHD were diagnosed by a psychiatrist according to the Conners adult ADHD diagnostic interview for DSM-IV-TR (CAADID) (Conners, Epstein, & Johnson, 2001).
Results
Table 1 shows the demographic data, P50 parameters and SGI scores.
Age, Sex and Educational Level were not significantly different between the three groups.
The mean ASRS overall score for adults with ADHD was 51.62 (SD = 8.07), ASRS inattention score was 28.25 (SD = 4.54) and ASRS hyperactivity score was 23.37 (SD = 6.21). Eight patients (33%) were medicated with methylphenidate. The mean dose was 31.5 mg (SD = 8.33).
The PANSS overall score for the patients with schizophrenia was 76.6 (SD = 21.3), the
Discussion
To our knowledge, this is the first study that investigated both P50 suppression and abnormal perceptual experiences related to sensory gating within the same group of adults with ADHD.
Concerning P50 suppression, the main result of the present study was that adults with ADHD exhibited a significant P50 suppression deficit in a dual click conditioning-testing paradigm compared to healthy subjects, as did patients with schizophrenia. This finding indicates the inability to filter intrusive
Conflict of interest statement
The authors declare no conflicts of interest.
Acknowledgments
We acknowledge Adeline Surray and Christelle Berthet for their technical assistance in the ERP recordings and Zohra Brandejsky for her comments. This work was supported by CNRS (Centre National de la Recherche Scientifique).
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