Sensory gating in adult with attention-deficit/hyperactivity disorder: Event-evoked potential and perceptual experience reports comparisons with schizophrenia

doi:10.1016/j.biopsycho.2015.03.002

Biological Psychology

Volume 107, April 2015, Pages 16-23

https://doi.org/10.1016/j.biopsycho.2015.03.002 Get rights and content

Highlights

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Adults with attention-deficit/hyperactivity disorder (ADHD) report perceptual inundation.
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Adults with ADHD had significantly higher scores on the Sensory Gating Inventory (SGI), a validated scale.
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Adults with ADHD had significantly lower P50 suppression than healthy subjects.
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Adults with ADHD had sensory gating deficit.
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The SGI and P50 suppression data are correlated.
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These deficits were similar to those found in patients with schizophrenia.

Abstract

Background

In daily life, adults with attention-deficit/hyperactivity disorder (ADHD) report abnormal perceptual experiences that can be related to sensory gating deficit. This study investigated and compared P50 suppression (a neurophysiological measure of sensory gating) and perceptual abnormalities related to sensory gating deficit in ADHD and schizophrenias patients.

Methods

Three groups were compared: 24 adults with ADHD, 24 patients with schizophrenia and 24 healthy subjects. The Sensory Gating Inventory (SGI), a validated self-report questionnaire, was used to measure perceptual abnormalities related to sensory gating deficit. P50 suppression was measured by P50 amplitude changes in a dual-click conditioning-testing auditory event-related potential procedure.

Results

Adults with ADHD had significantly higher scores on the SGI and significantly lower P50 suppression than healthy subjects. These deficits were similar to those found in patients with schizophrenia. A correlation was found between both the SGI and P50 suppression data in adults with ADHD and patients with schizophrenia.

Discussion

The findings confirm previous results found in patients with schizophrenia. Moreover, adults with ADHD, similar to patients with schizophrenia, had abnormal P50 suppression and reported being flooded with sensory stimuli. Abnormal neurophysiologic responses to repetitive stimuli gave rise to clinically abnormal perceptions.

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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As determined by confirmatory factor analysis, the SGI has a four-factor structure, with domains for Perceptual Modulation; Distractibility; Over-Inclusion and Hyperawareness; and Fatigue and Stress Vulnerability. [65] Notably, SGI scores correspond with neurophysiologic markers of sensory gating impairment (see Section 4, ‟Discussion”) in schizophrenia [67] and ADHD. [68,69] We quantified severity of obsessive-compulsive and ADHD symptoms with validated self-report measures (Table 1).
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SOR is prevalent in adults with CTD and in adults with OCD but does not significantly differ in magnitude between these disorders. Across CTD, OCD, and healthy control adult populations, SOR is independently associated with both obsessive-compulsive and ADHD symptoms, suggesting a transdiagnostic relationship between these sensory and psychiatric manifestations. Future cross-disorder, longitudinal, and translational research is needed to clarify the role and prognostic import of SOR in CTDs, OCD, and other neurodevelopmental disorders.
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Among healthy adults, a previous study found that Perceptual Modulation was correlated with P50 SG ratios, while Over-Inclusion was more associated with N100 SG ratios, thereby suggesting that individuals with more self-reported disturbances in perceptual modulation would exhibit poorer cortical SG function [13]. Furthermore, in patients with ADHD, P50 SG ratios were significantly correlated with Perceptual Modulation, Distractibility, Over-Inclusion, and total SGI scores [8]. Similarly, in patients with schizophrenia, those with larger P50 SG ratios demonstrated higher scores on the SGI as predicted [6].
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Twenty-two healthy young adults performed the auditory paired-stimulus paradigm during magnetoencephalographic recordings. SG of M50 and M100 was measured as ratios (S2/S1) and differences (S1–S2). They were also evaluated with SGI, which factored into three categories of Perceptual Modulation, Distractibility, and Over-Inclusion. SG in the STG, IFG, and IPL were compared between left and right hemispheres, and were used to determine the relationship with SGI.
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Similarly, P50 gating deficits are found in several psychiatric disorders such as schizophrenia (e.g. Adler et al., 1982; Braff et al., 2007; Aggernaes et al., 2010), PTSD (e.g. Gillette et al., 1997; Holstein et al., 2010) and Alzheimer's dementia (Thomas et al., 2010). Only few previous studies have explored P50 suppression in adult ADHD patients, with inconsistent results (Olincy et al., 2000; Holstein et al., 2013; Micoulaud-Franchi et al., 2015). However, all the above mentioned ADHD studies on PPI and P50 suppression included patients with either current or previous medical treatment with psychostimulants, usually methylphenidate (MPH, which among others increases dopamine signaling), or with comorbid symptoms which may have influenced results: There is evidence for the involvement of – both increased as well as decreased – dopaminergic neurotransmission in PPI (Feifel, 1999; Swerdlow et al., 2003; Oranje et al., 2004a; Hanlon et al., 2009), as well as in P50 suppression (e.g. Oranje et al., 2002; Csomor et al., 2008).
Deficient information processing in ADHD theoretically results in sensory overload, which in turn may underlie its symptoms. If this sensory overload is caused by deficient filtering of environmental stimuli, then one would expect finding deficits in P50 gating and prepulse inhibition of the startle reflex (PPI). Previous reports on these measures in ADHD have shown inconsistent findings, which may have been caused by either medication use or comorbidity (e.g. ASD). The primary aim of this study was therefore to explore P50 suppression and PPI in adult, psychostimulant-naïve patients with ADHD without major comorbidity, and to examine the effects of 6 weeks treatment with methylphenidate (MPH) on these measures.
A total of 42 initially psychostimulant-naive, adult ADHD patients without major comorbidity and 42 matched healthy controls, were assessed for their P50 gating, PPI, and habituation/sensitization abilities at baseline and after 6 weeks of treatment with methylphenidate.
Although six weeks of treatment with MPH significantly reduced symptomatology as well as improved daily life functioning in our patients, it neither significantly affected PPI, P50 suppression nor sensitization, but habituation unexpectedly decreased.
The absence of PPI and P50 suppression deficits in our patients in the psychostimulant-naïve state indicates no gating deficits. In turn, this suggests that the difficulties to inhibit distraction of attention by irrelevant stimuli that many patients with (adult) ADHD report, have a different origin than the theoretical causes of sensory overload frequently reported in studies on patients with schizophrenia.

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Sensory gating in adult with attention-deficit/hyperactivity disorder: Event-evoked potential and perceptual experience reports comparisons with schizophrenia

Highlights

Abstract

Background

Methods

Results

Discussion

Introduction

Section snippets

Participants

Results

Discussion

Conflict of interest statement

Acknowledgments

Biological Psychiatry

Biological Psychiatry

Biological Psychiatry

Biological Psychiatry

Biological Psychiatry

Schizophrenia Research

Biological Psychiatry

Neuroscience & Biobehavioral Reviews

Psychiatry Research

Biological Psychiatry

Psychiatry Research

Biological Psychiatry

Clinical Neuroscience Research

Biological Psychiatry

Schizophrenia Research

Psychiatry Research

Biological Psychiatry

Schizophrenia Research

Biological Psychiatry

Psychiatry Research

Encephale

Sleep Medicine

Normalization of auditory physiology by cigarette smoking in schizophrenic patients

The American Journal of Psychiatry

Neurophysiological evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia

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Sensorimotor gating and schizophrenia. Human and animal model studies

Archives of General Psychiatry

Prevalence and correlates of attention deficit hyperactivity disorder in adults from a French community sample

The Journal of Nervous and Mental Disease

Sensory gating deficits assessed by the P50 event-related potential in subjects with schizotypal personality disorder

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Medical Care