Electrophysiological evidence of enhanced distractibility in ADHD children

Transcription

1 Neuroscience Letters 374 (2005) Electrophysiological evidence of enhanced distractibility in ADHD children V. Gumenyuk a,, O. Korzyukov a,b, C. Escera c,m.hämäläinen d, M. Huotilainen a,e,f, T. Häyrinen d, H. Oksanen d,r.näätänen a,e, L. von Wendt d, K. Alho g a Cognitive Brain Research Unit, Department of Psychology, University of Helsinki, Helsinki, Finland b Department of Psychiatry, Yale University and VA-Connecticut Healthcare System, West Haven, CT, USA c Cognitive Neuroscience Research Group, Department of Psychiatry and Clinical Psychology, Faculty of Psychology, University of Barcelona, Catalonia, Spain d Department of Child Neurology, Hospital for Children and Adolescents, Helsinki University Central Hospital, Helsinki, Finland e Helsinki Brain Research Centre, Helsinki, Finland f Collegium of Advanced Studies, University of Helsinki, Finland g Department of Psychology, University of Helsinki, Helsinki, Finland Received 28 June 2004; received in revised form 14 October 2004; accepted 21 October 2004 Abstract Abnormal involuntary attention leading to enhanced distractibility may account for different behavioral and cognitive problems in children with attention deficit hyperactivity disorder (ADHD). This was investigated in the present experiment by recording event-related brain potentials (ERPs) to distracting novel sounds during performance of a visual discrimination task. The overall performance in the visual task was less accurate in the ADHD children than in the control children, and the ADHD children had a higher number of omitted responses following novel sounds. In both groups, the distracting novel sounds elicited a biphasic P3a ERP component and a subsequent frontal Late Negativity (LN). The early phase of P3a ( ms) had significantly smaller amplitudes over the fronto-central left-hemisphere recording sites in the ADHD children than in the control group presumably due to an overlapping enhanced left-hemisphere dominant negative ERP component elicited in the ADHD group. Moreover, the late phase of P3a ( ms) was significantly larger over the left parietal scalp areas in the ADHD children than in the controls. The LN had a smaller amplitude and shorter latency over the frontal scalp in the ADHD group than in the controls. In conclusion, the ERP and behavioral effects caused by the novel sounds reveal deficient control of involuntary attention in ADHD children that may underlie their abnormal distractibility Elsevier Ireland Ltd. All rights reserved. Keywords: Attention deficit hyperactivity disorder; Distraction; Children; Orienting; P3a; Reorienting negativity (LN/RON) Attention deficit hyperactivity disorder (ADHD) is a multidimensional disorder that has its onset in childhood and that is characterized by persistent problems of inattention, impulsivity, and hyperactivity [2,15]. In ADHD patients, difficulties with sustained attention tasks [11] can be caused by different alternatives, one being abnormal distractibility. Therefore, the present study compared involuntary attention and distractibility in ADHD and Corresponding author. Tel.: ; fax: address: valentina.gumenyuk@helsinki.fi (V. Gumenyuk). healthy children, as indicated by distraction of visual task performance by task-irrelevant novel sounds and by eventrelated brain potentials (ERPs) to these sounds. Highly deviant, task-irrelevant auditory and visual stimuli elicit a P3 component of ERP called the P3a or novelty P3 [5,21]. The P3a is maximal over the fronto-central scalp, and therefore, it can be separated from the parietally maximal P300 or P3b response to auditory and visual target stimuli. The P3a has been suggested to be associated with the orienting response [5,6,13,20] and with detection and evaluation of novelty [7]. Association of P3a with involuntary attention /$ see front matter 2004 Elsevier Ireland Ltd. All rights reserved. doi: /j.neulet

2 V. Gumenyuk et al. / Neuroscience Letters 374 (2005) switching is evidenced by the fact that P3a-eliciting novel sounds also distract visual task performance in adults [6] and children [9]. The P3a to novel sounds has two phases: an early phase (ep3a) peaking at ms and a late phase (lp3a) peaking at ms from sound onset [6]. In adults, the ep3a has its maximum amplitude over the central scalp, whereas the lp3a is distributed widely and has its maximum over the frontal scalp. According to scalp current density analysis [25], magnetoencephalography [1], and studies in patients with local brain lesions [14], the ep3a is generated in the auditory and temporo-parietal cortices, while the lp3a gets a major contribution from the prefrontal cortex [13,25]. Thus, multiple brain areas are involved in involuntary attention and auditory novelty detection. This appears to be true also in children. The scalp distributions of the ep3a and lp3a to novel sounds in children aged over 11 years are similar to those in adults [9]. However, in 7 10-year-olds, the lp3a has its maximum over the centro-parietal scalp suggesting that the auditory attention networks are not yet fully developed at this age [9]. The P3a to distracting sounds is followed by a reorienting negativity (RON) component in adult ERPs [19] and the Late Negativity (LN) in children [9]. RON and LN have maximum amplitudes over fronto-central scalp areas at ms after onset of a distracting sound and may be associated with the prefrontal brain mechanisms involved in reorienting attention back to task performance after a distracting event [9,19]. Previous studies found no differences between ADHD and control children in P3a responses to novel visual stimuli [10,11]. However, Kemner et al. s [11] data suggest smaller P3a responses over the parietal scalp to task-irrelevant novel sounds in ADHD children than in healthy controls, although this effect did not reach statistical significance. In contrast, Kilpeläinen et al. [12] found enhanced frontal P3 deflections (presumably the P3a) in distractible children in comparison with non-distractible children in response to infrequent target tones occurring among frequent tones. In the present study, we investigated these issues further by recording ERPs to repeating tones and novel sounds from ADHD children and healthy controls while they concentrated on a demanding visual task. Eleven 8 10-year-old ADHD and 10 age-matched healthy children were studied. One ADHD child was excluded due to a very poor performance (less than 50% hits) in the visual discrimination task (see below). The remaining ADHD group and the control group consisted of 10 subjects each (mean ages 8.7 and 8.6 years., respectively; one girl in each group). The ADHD children were recruited from the Department of Child Neurology of the Helsinki University Central Hospital. All of them had a thorough multidisciplinary diagnostic assessment and all fulfilled the DSM-IV [2] criteria for ADHD and had no other comorbidity disorders. Those ADHD children who were on medication were withdrawn from it at least a day before the experiment. The general intellectual ability of the clinical group was assessed with Wechsler s [22,23] intelligence scales. All children in the ADHD group had their verbal, performance, and full-scale intelligence quotients (IQ) within the normal range (means: 108, 100, and 104, respectively). The ADHD children were rewarded with a ticket to a self-chosen movie (according to the protocol). The control children were recruited from ordinary primary schools (none of the control children were in gifted programs at school) and were rewarded for their participation with 6D. None of the control children had any diagnosed psychological or neurological problems. All of them were in the ageappropriate grade at school. All children had a normal or corrected-to-normal vision and normal hearing. Written informed consents were obtained from all parents of children participating in the study. The Ethics Committee of the Hospital for Children and Adolescents approved the protocol of the present study for the ADHD children and The Ethical Committee of the Department of Psychology, University of Helsinki, approved the protocol of the present study for the control group. The children were presented with auditory-visual stimulus pairs at a constant rate of one pair in every 1.7 s. Each sound had a duration of 200 ms and was delivered binaurally through headphones at 50 db SPL. The sound was either a sinusoidal tone of 600 Hz (P = 0.80; or 560 tones) or one of the complex environmental novel sounds presented randomly (P = 0.20) with the exception that at least 3 tones occurred between any two successive novel sounds. The novel sounds were drawn from a pool of 140 different environmental sounds, such as those produced by a hammer, rain, and car horn. Each novel sound was presented only once during the experiment. The visual stimuli were 32 different white-line drawings (16 animals and 16 non-animals) extending 9 cm horizontally and vertically, presented for 300 ms, and starting at 300 ms after the onset of the preceding sound. The drawings were displayed in a random order in the center of a black computer screen located approximately 130 cm from the subject s eyes. The children were instructed to ignore the sounds, to focus their gaze on a white fixation cross (1 cm 1 cm) continuously presented at the center of the screen, and to respond as accurately as possible by pressing one response button with their right thumb to an animal image appearing on the screen and another button with their left thumb to a non-animal image. The children s motivation to perform the task was indicated by their genuine interest to their hit rate reported to them after each block. The electroencephalogram (EEG; Hz, sampling rate 250 Hz) was recorded from frontal (Fp1, Fp2, F7, F3, Fz, F4, and F8), central (C3, Cz, C4), temporal (T3, T4, T5, T6), parietal (P3, Pz, P4), and occipital (O1, O2) scalp sites and from the left and right mastoids (LM and RM, respectively). Voltage changes caused by eye movements and blinks were monitored with recordings from the forehead sites (Fp1, Fp2) and from additional electrodes placed at the left and right canthi. The common reference electrode was placed at the tip of the nose. ERPs were obtained separately for the tones and novel sounds by averaging EEG epochs over a 900 ms pe-

3 214 V. Gumenyuk et al. / Neuroscience Letters 374 (2005) riod starting 100 ms before each sound onset. These EEG epochs were digitally band-pass filtered at 1 30 Hz. Epochs with extracerebral artifacts exceeding ±100 V at any electrode were excluded from averaging. Also, the epochs for the first four stimuli of each block and the epochs for any tone occurring right after a novel sound were excluded. For each child, averaged ERPs to tones and novel sounds consisted of at least 380 and 90 acceptable EEG epochs, respectively. Because the children were instructed to perform the visual discrimination task with an accuracy instruction (stress on performance accuracy, not on speed, cf. [17]), changes in the rates of correct responses ( hits ) and incorrect responses (wrong button presses and response omissions) caused by the task-irrelevant novel sounds were used as major behavioral indexes distractibility. A correct button press given ms after visual stimulus onset was classified as a hit. Within-group difference of means rates of hit, wrong and missed responses, and hit reaction times (RTs) were analyzed with t-tests, while betweengroup difference of those were analyzed with Mann Whitney U-test (depended variables: tone versus novel). The P3a and LN amplitudes were measured from ERP difference waves obtained by subtracting ERPs to tones from those to novel sounds [6,9]. Their amplitudes were measured as mean voltages over fixed latency windows determined after visual inspection of the grand-average ERP difference waves at Fz and Cz electrodes. The mean amplitudes of the ep3a and lp3a were measured over and ms from sound onset, respectively, in relation to the mean difference-wave amplitude during the 100 ms prestimulus baseline. The LN amplitudes, in turn, were measured over two latency windows: and ms. Between-group differences in the P3a and LN amplitudes were examined with ANOVAs and Newman Keuls post hoc tests. Greenhouse Geisser corrections were used for the P-values when appropriate. ANOVAs for the ep3a and lp3a, included electrode factors Frontality (frontal F3, Fz, F4 versus central C3, Cz, C4 versus parietal P3, Pz, P4 electrodes) and Laterality (left-hemisphere F3, C3, P3 versus midline Fz, Cz, Pz versus right-hemisphere F4, C4, P4 electrodes). Table 1 shows mean RTs, and the mean rates of hits, wrong responses, and response omissions in the visual task for the ADHD and control groups. In both groups, the distraction effect in the visual task caused by novel sounds was significant: An occurrence of a novel sound decreased the number of correct responses to the following visual stimulus, in comparison with visual stimuli preceded by a tone both in the ADHD and control groups (t(9) = 2.54; P < 0.03; t(9) = 2.96; P < 0.01, respectively). Both groups showed longer RTs after novel sounds than after tones, but this effect reached significance only in the controls (t(9) = 3.79; P < 0.004). A Mann Whitney U-test for the hit rates yielded a significant between-group differences in the visual-task accuracy both for the visual stimuli preceded by a tone (U(11) = 2.9; P < 0.002) and for those preceded by a novel sound (U(14) = 2.7; P < 0.005), indicating that ADHD chil- Table 1 Mean (standard deviations in parentheses) RTs, hit rates, wrong-response and miss rates of the ADHD and control children in performing the visual discrimination task after an occurrence of a task-irrelevant tone vs. novel sound Performance Stimulus ADHD mean (S.D.) Controls mean (S.D.) RT (ms) Tone 476 (78) 498 (122) Novel 488 (86) 553 (142) Hit rate (%) Tone 65 (13) 81 (8) Novel 62 (12) 78 (10) Wrong-response (%) Tone 13 (5) 6 (3) Novel 12 (6) 9 (3) Miss-response (%) Tone 22 (9) 12 (10) Novel 26 (9) 13 (10) dren had an overall smaller percentage of correct responses than the controls. A Mann Whitney U-test for the rate of missed responses indicated that an occurrence of a novel sound (in comparison with an occurrence of a tone) enhanced significantly more the number of response omissions in the ADHD children than in the controls (U(17) = 2.49; P < 0.01), this effect of the preceding sound on the number of omissions being 4% in the ADHD group but only 1% in the control group (see Table 1). No significant group difference or effect of preceding stimulus was found for the number of wrong responses. Fig. 1 displays grand-average ERPs elicited by the auditory-visual stimulus pairs. In the ADHD and control groups, tones elicited only a small auditory N1 component (peak around 100 ms from sound onset at the Cz electrode), presumably due to a relative immaturity of the auditory cortex [18]. A P3a response was elicited by novel sounds in each age group (Fig. 1). Fig. 2 shows the grand-average ERP difference waves of the P3a and LN responses to the novel sounds for the ADHD and control groups. Consistent with our previous studies in healthy children [9], the P3a had a biphasic structure. As seen in Fig. 2, the ep3a was largest over the fronto-central scalp in both groups, whereas the lp3a had a wider distribution over the midline scalp areas. An ANOVA for the ep3a amplitudes at F3, FZ, F4, C3, Cz, C4, P3, Pz, and P4 electrodes indicated a significant Group Frontality Laterality interaction (F(4,72) = 4.64; P < 0.01). Subsequent Newman Keuls tests showed that this was due to an amplitude difference between the groups over the frontocentral left-hemisphere for the ep3a: as seen in Figs. 2 and 3a, the ADHD children had smaller ep3a amplitudes than did the controls (mean amplitude measured at ms: 0.9 versus 3.35 V at F3, and 0.9 versus 3.27 V at C3, respectively; P < 0.04 for both comparisons). As seen in Fig. 2 (e.g., the F3 electrode), this effect might be caused by an overlapping negative component peaking around 240 ms in ADHD children and reducing their ep3a amplitudes over the left frontal scalp. The left-frontal scalp distribution of this possible negative component is seen in Fig. 3b showing a

4 V. Gumenyuk et al. / Neuroscience Letters 374 (2005) Fig. 1. Grand-average ERPs elicited by tones (solid line) and novel sounds (dashed line) at selected electrodes in the ADHD and control children. Note that the auditory ERPs are followed and partially overlapped by the ERPs to the subsequent visual stimulus (visual-stimulus onset indicated by vertical dashed line). distribution map for the amplitude difference between the grand-average novel-minus-tone ERP difference waves of the ADHD and control group at ms from sound onset. An ANOVA for the lp3a revealed a significant Group Frontality Laterality interaction (F(4,72) = 2.56; P < 0.04). According to the subsequent Newman Keuls tests, the ADHD children had significantly larger lp3a amplitudes at the left and midline parietal scalp sites (4.8 versus 3 Vat P3, P < 0.03; 6.7 versus 4.6 V at Pz; P < 0.01). This effect is seen in Figs. 2 and 3a. Following the P3a, a frontal LN was observed in both groups (Figs. 2 and 3a). The LN appeared to be smaller in amplitude and to peak earlier in the ADHD group than in the controls. Therefore, the LN amplitudes were measured at frontal electrode sites (F8, F4, Fz, F3, F7) as mean voltages over two time windows, i.e., over and ms from sound onset. The earlier of these windows covers the peak latency of the LN in the grand-average ERP difference waves of the ADHD group and the later window covers the peak latency of the LN of the control group. An ANOVA for these LN amplitudes including factors Group, Laterality (F8 versus F4 versus Fz versus F3 versus F7) and Time Window ( ms versus ms) revealed a significant Group Laterality Time Window interaction (F(4,72) = 6.18; P < 0.002) caused by the fact that over the frontal midline, the LN was larger in amplitude in the ADHD group than in the controls during the earlier time window (mean amplitudes 2.8 V versus 1.2 V, respectively; Newman Keuls test: P < 0.001) but smaller in the ADHD group than in the controls during the later time window (mean amplitude 0.01 V versus 1.7 V, respectively; P < 0.001). Fig. 2. Grand-average ERP difference waves obtained by subtracting the ERPs to tones from those to novel sounds. The P3a elicited by novel sounds consists of two phases: the ep3a and lp3a, which are followed by the LN.

5 216 V. Gumenyuk et al. / Neuroscience Letters 374 (2005) Fig. 3. (a) P3a and LN scalp-distribution maps for each group of children. The maps show average voltages of novel-minus-tone ERP difference waves (see Fig. 2) at the latency ranges of the ep3a, lp3a, and the earlier and later phases of LN. (b) Topographic maps of the ERP difference between the ADHD and control groups (ADHD minus control) suggesting abnormal brain activity in the left-hemisphere of the ADHD children peaking around 240 ms. In conclusion, the present performance data are in accordance with our previous studies [9] by showing that novel sounds distract children s performance in a visual discrimination task as indicated by decreased hit rates and increased RTs after an occurrence of a novel sound in comparison with occurrence of a repeating tone. Moreover, larger number of response omissions after a novel sound in the ADHD group than in the control group revealed higher distractibility in the ADHD group. Abnormal involuntary attention in the ADHD children was also supported by the ERPs to the distracting novel sounds. These sounds elicited a biphasic P3a response with an early phase (ep3a) that had significantly smaller amplitude over the left-hemisphere in the ADHD children than in the control group. Thus, reduced ep3a amplitudes in the ADHD were presumably caused by a left-hemisphere dominant negative ERP component evoked by the novel sounds in the ADHD group but not in the control group or evoked with much smaller amplitudes in the latter group. Alternatively, the abnormal left-hemisphere activity in the ADHD children around 240 ms from novel-sound onset might be caused by a genuine reduction in the activity of one of the left-hemisphere generator sources contributing to the P3a response at the latencies between the ep3a and lp3a peaks (cf. [25]). For example, this reduction might be associated with a deficit in controlling verbalized encoding of these distracting environmental sounds that may be based on automatic stimulus identification and classification [6]. Moreover, the lp3a showed enhanced amplitudes in the ADHD group in comparison with the controls in parietal electrode sites especially over the lefthemisphere. These findings are in agreement with previous findings showing differences between ADHD and controls at left-hemisphere sites to auditory stimulus changes in ADHD patients compared with control subjects [16]. Interestingly, Gomot et al. [8] reported in 5 9-year-old autistic children concentrating on watching a silent movie atypical activity elicited by frequency changes in a repeating sound. This activity occurred at the latency of the mismatch negativity (MMN) and was localized with scalp current density analysis to the left frontal cortex. Their study together with the present results suggests left-hemisphere abnormality that may underlie various attentional problems in children. Finally, in the present study, the lp3a was followed by the LN component that had a smaller amplitude and shorter latency in the ADHD children than in the controls. In healthy children, the LN has been interpreted to correspond the reorienting negativity (RON) observed in adults and proposed to be generated by prefrontal mechanisms involved in reorienting of attention back to the distracted task performance [3,9,19,24]. Therefore, the reduced LN in the ADHD chil-

6 V. Gumenyuk et al. / Neuroscience Letters 374 (2005) dren might be associated with a prefrontal cortical dysfunction [4] leading to problems in reorienting attention back to the distracted task performance. This problem in reorienting attention is indicated in the present study by enhanced number of omitted responses in the visual task after a novel sound. The decrement in the LN peak latency observed in the ADHD children in relation to the controls might, in turn, be associated with a higher degree of impulsivity, which is a symptom of ADHD [2,15]. In summary, the present study suggests that ERPs recorded to the task-irrelevant novel stimuli distracting the children s performance provide us with evidence supporting the observations of attentional and behavioral deficits in ADHD. Although, the present study should be considered as preliminary, given the relatively small size of the two groups, the present results suggest that a multimethodological approach combining neuropsychological, behavioral and electrophysiological measures of distractibility and involuntary orienting of attention improve our understanding of the brain behavior relationship in ADHD. Acknowledgements The authors thank Ms. Kirsi Järvinen for her help in recruiting the control children, as well as Ms. Leena Wallendahr and Mr. Timo Saarinen for assistance with the electrophysiological recording. V. Gumenyuk was supported by the Academy of Finland grant no R. Näätänen and O. Korzyukov were supported by the Academy of Finland grants nos and C. Escera was supported by the grant no. PM of the Spanish Ministry of Science and Technology. References [1] K. Alho, I. Winkler, C. Escera, M. Huotilainen, J. Virtanen, I.P. Jääskeläinen, E. Pekkonen, R.J. 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