Attention deficit and hyperactivity disorder (ADHD) is a neurodevelopmental disorder that is characterized by inappropriate levels of inattention, hyperactivity, and/or impulsivity (American Psychiatric Association, 2013). Although it was often seen as a disorder that only affects children, around 60% of cases report symptom persistence in adulthood (Sibley et al., 2017). Whereas hyperactivity and impulsivity are often the main symptoms in children and decrease with increasing age, adults are mostly affected by inattention (Uchida et al., 2015). While ADHD research mainly focuses on the core symptoms and their neuronal underpinnings, the basic and important area of reception and processing of stimuli is rarely examined (Schulze et al., 2020).

Sensory processing describes the nervous systems ability to receive, modulate, integrate, and organize external stimuli in order to generate an appropriate response to the environment (Hebert, 2015). There is evidence that sensory processing of several modalities in people with high scores in the adult ADHD self-report scale (ASRS) is deficient compared to those with low ASRS scores (Panagiotidi et al., 2018). Sensory processing of adults with ADHD is marked by higher scores in sensory sensitivity, low registration, and sensory avoiding behavior. At the same time, sensation seeking behavior scores are found to be either higher or lower (Bijlenga et al., 2017; Kamath et al., 2020). Modality specific impairment in sensory processing have mainly been reported for vision and audition (Schulze et al., 2020). On the behavioral level, patients report an auditory hypersensitivity which is reflected in higher distractibility from sounds, e.g., the inability to suppress background noises like a ticking clock and overinclusion of auditory stimuli (Faraone et al., 2000; Panagiotidi et al., 2017). Visual processing has shown to be deficient as well, indicated by worse perception of depth and higher distractibility (Panagiotidi et al., 2017), worse temporal allocation of visual attention (Hollingsworth et al., 2001) and slower response times in a compound search task (Cross-Villasana et al., 2015).The underlying principles of these perceptional sensitivities are far from understood, but evidence is pointing to inhibitory and modulatory deficits at early stimulus processing capacities (Micoulaud-Franchi et al., 2019).

Early stimulus processing can be measured electrophysiologically, for example, by means of event-related potentials (ERPs; Barry et al., 2009). For instance, the P200 component that is the peak positivity that occurs between 175 and 250 ms after a stimulus onset, is associated with early sensory processing steps including like stimulus registration, encoding, evaluation, and discrimination, early attentive mechanisms and selective attention, as well as the inhibition of further processing of competing information (Näätänen, 1992; Korostenskaja et al., 2008; Barry et al., 2009; Lazzaro et al., 2009; Sur and Sinha, 2009; Stefanou et al., 2020). This component has been reported to be deficient in patients with ADHD, showing an upregulation (Barry et al., 2009).

When a person, neurotypical as well as on the ADHD spectrum, is confronted with stimuli of a certain sensory modality (e.g., auditory information), the other senses are also co-activated (e.g., visual cortices; Molholm et al., 2002; McDonald et al., 2013; Hillyard et al., 2016). This co-activation, also called crossmodal activation has been reported in several modalities, especially between the auditory and visual domain (Hillyard et al., 2016). It is well documented that primary auditory and visual cortices are anatomically connected and influence each other already at early stages of sensory processing (Falchier et al., 2002; Molholm et al., 2002; Schroeder et al., 2003; Komura et al., 2005). For example, Hillyard et al. (2016) reported improved detection and discrimination of a visual stimulus resulting from a preceding auditory tone (Korostenskaja et al., 2008).

These audiovisual perceptual modulations further correlate with EEG phenomena, such as the auditory-evoked contralateral occipital positivity (ACOP). It describes a net positivity that occurs in the contralateral occipital electrodes 250–400 ms after the presentation of a sound. A recent study shows that the ACOP reflects facilitated visual processing and therefore might indicate an involuntary reallocation of attentional resources to the visual domain, as proposed by Hillyard et al. (2016) (Keefe et al., 2021).

Recent evidence points to the fact that crossmodal sensory processing might be deficient in people with ADHD (Salmi et al., 2018). Salmi et al. (2018) examined auditory and visual attentional mechanisms in adults with ADHD using fMRI and measured a higher crossmodal visual activation in a unimodal focused auditory attention task compared to controls. However, given the low temporal resolution of fMRI, it is difficult to disentangle whether those activations are the result of early sensory processing or attentional mechanisms. Therefore, in the current study, we used, for the first time, electroencephalography to identify a potential abnormal regulated crossmodal activation in adult ADHD. To provoke a potential crossmodal response for unisensory stimuli, we performed an auditory and visual discrimination task separately. Since prior research shows deficient inhibitory activity at early sensory EEG components like P50, P100, and P200, we assume crossmodal spreading of sensory information. We hypothesize that adults with ADHD show higher auditory to visual crossmodal activations.

This is the first study addressing sensory crossmodal electrophysiological activity in adults with ADHD. In the auditory discrimination task, patients with ADHD showed a significantly enhanced crossmodal P200 amplitude and a significantly increased intramodal N200 amplitude compared to the healthy control group. No significant differences were found at earlier latencies. In the visual discrimination task, the patient group showed a significantly lower intramodal P50 at the channels O1 and O2 that represent intramodal sensory processing. At the channel Fz which represents crossmodal visual processing, the N100 component amplitude was significantly lower in the patient group compared to the healthy controls.

No other significant group differences of P50, P100, N100, P200, and N200 components were found. On the behavioral level, subjects with ADHD showed weaker auditory performances compared to the control group, although not reaching a statistical significance. In the visual discrimination task, the patient group also showed slightly but not significantly poorer performances.

Physiologically, the visual and auditory cortex are anatomically connected and influence each other already at early stages of sensory processing (Falchier et al., 2002; Molholm et al., 2002; Schroeder et al., 2003; Komura et al., 2005). The early crossmodal influence was found in the healthy control group at the crossmodal visual N100. This interaction is well measurable by a robust ERP component that is elicited in the visual cortex contralateral to a preceding laterally-presented sound after 250–400 ms. On the behavioral level, these spatially specific elicited sounds participate in visual perceptual alterations such as improved and faster discrimination, higher subjective intensity as well as the crossmodal reallocation of attentional resources to the visual domain (Retsa et al., 2020). In a study by Retsa et al., who investigated the conditions for the enhanced crossmodal visual activity to be measurable and concluded that it is dependent on the sounds’ spatial specificity. According to the authors, this dependency might indicate that early audiovisual crossmodal influences are only beneficial if the sound helps in selective visual attention processes, which are not required if the sounds are central and unspecific. Furthermore, it can be deduced that the suppression of crossmodal activations is equally important since they might lead to unnecessary spreading of attentional resources (Retsa et al., 2020).

In this study, we investigated auditory to visual crossmodal activations in ADHD by comparing the inter-group difference of the occipital P200 amplitude that was measured after the elicitation of a non-spatially specific sound. In general, the P200 component is associated with a number of early sensory processing steps including stimulus registration, discrimination, early attentive mechanisms as well as the inhibition of further processing of competing information (Näätänen, 1992; Korostenskaja et al., 2008; Barry et al., 2009; Lazzaro et al., 2009; Sur and Sinha, 2009; Stefanou et al., 2020). Until now, the P200 component has only been investigated at intramodal channels such as Fz and Cz in adults with ADHD (Micoulaud-Franchi et al., 2019), not at channels that can capture crossmodal activity. In the current study, the intramodal P50 and P200 component amplitudes between adults with ADHD and healthy controls did not differ significantly, which is in line with the results of Micoulaud-Franchi et al. (2019).

They were also able to show that the P50 component is related to later sensory processing, marked by a decreased P300 component that correlates with higher distractibility scores in the Sensory Gating Inventory. We found a higher intramodal auditory N200 and an enhanced crossmodal P200 component, indicating enhanced visual activity during the auditory discrimination task. This occipitally enhanced P200 component we measured in adults with ADHD can be related to the enhanced crossmodal visual activity in healthy populations that was mentioned before. One interpretation for the intergroup difference is that enhanced intra-and crossmodal auditory activity in ADHD reflects increased neuronal sensitivity in the processing of auditory stimuli and more sensory registration in the visual domain and thus more spreading of attentional resources, pointing toward deficient stimuli related inhibitory mechanisms in adults with ADHD. Our results are supported by the study of Salmi et al. (2018) who proposed that altered attentional processing in the auditory domain might result from enhanced visual activity.

The lack of significant ERP amplitude differences in the visual discrimination task indicates that early visual sensory processing of low saliency stimuli such as Gabor patches is not impaired in adults with ADHD. Still, there is evidence that visual processing does not function properly in patients with ADHD. While we investigated possible aberrancies in early stages of sensory processing, Cross-Villasana et al. (2015) measured delayed posterior contralateral negativity waves in adults with ADHD, indicating slower attentional selection in later stages of sensory processing. In addition to the impairment of unimodal visual processing in adults with ADHD, there is evidence that multisensory integration processes are aberrant as well, which were not investigated in this study (Schulze et al., 2020, 2021, 2022).

In the current study, subjects with ADHD had higher auditory discrimination thresholds, made more mistakes and it took them more trials to reach their minimal threshold compared to the healthy controls, despite not reaching a statistical significance (see Figures 3C,D). Fostick (2017) investigated auditory behavior in adults with ADHD by measuring their time order judgment (TOJ) thresholds and found that unmedicated adults with ADHD show significantly higher TOJ thresholds, whereas medicated patients had similar TOJ thresholds compared to the control group. This group difference of TOJ thresholds indicates (American Psychiatric Association, 2013) deficient auditory processing and (Sibley et al., 2017) that MPH might adjust the neuronal spreading to a similar degree as in healthy controls (Fostick, 2017). Additionally, Taitelbaum-Swead et al. (2019) compared auditory behavior between ADHD patients and healthy controls by measuring their listening effort in an audiovisual dual-task paradigm. They found that the ADHD group had lower accuracy in auditory attention when a visual distractor was present, which might be due to the deficient allocation of attentional resources to the auditory domain (Taitelbaum-Swead et al., 2019).

In the current study, adults with ADHD performed worse, although not significant, in the auditory discrimination task.

Besides the crossmodal spreading, one reason for the worse auditory performance might be impaired sustained attention capabilities in the patient group, as it is well reported as a common symptom in adult ADHD (Faraone et al., 2000; Marchetta et al., 2007). Subjects of the patient cohort scored significantly higher in the domain “hypersensitivity” compared to healthy controls, which is also in line with the literature (Faraone et al., 2000; Fostick, 2017; Panagiotidi et al., 2017). Although an auditory hypersensitivity suggests better performances in auditory discrimination (Fostick, 2017), the underlying mechanisms that might explain the observed worse performance results are not yet disentangled. Possible Mechanisms for this observation are involuntary attentional shifts, crossmodal spreading of attentional resources as well as deficient inhibition mechanisms. As the results of other researchers show, early auditory processing deficits might indeed be a part of the pathophysiology of ADHD, although the performance differences we measured did not reach a statistical significance. It is therefore hard to make a definite deduction on the behavioral level and it is possible that there is no correlation between the significantly different EEG components and the task performances. Still, we observed that 10 of the 14 healthy subjects reached the smallest possible frequency interval between two tones after only 40% of all trials, which might be linked to a ceiling effect that results from the task design (see Table 5).

Further, higher sensory sensitivity goes along with less sensation seeking behavior, indicating lower sensory thresholds that lead to more auditory sensory registration. It is worth noting that the higher “low registration” scores (see Table 1) of the patient group do not contradict this enhanced auditory sensory registration, because the ASP results reflect sensory processing of all modalities, not just that of the auditory domain. This is in line with current studies that suggest a hypo- as well as hypersensitivity in different domains in people with ADHD (Kamath et al., 2020). Although our results do not show a significant group difference between the sensation seeking scores, we observed tendencies toward less sensation seeking behavior in subjects with ADHD (see Table 1).

The performance differences in the visual discrimination task between the groups are minor and therefore congruent with the lack of electrophysiological group differences. Both groups made more errors in the second half of the experiment, which can be interpreted considering increased difficultness for the contrast detection threshold. The lack of major effects strengthens the hypothesis that early visual sensory processing of low saliency stimuli like Gabor patches is not impaired in adults with ADHD. Still, there is evidence that aberrant visual processing leads to impaired visual performance in patients with ADHD, indicated by worse temporal allocation of visual attention (Hollingsworth et al., 2001), slower response times in a compound search task (Cross-Villasana et al., 2015), worse perception of depth, and higher distractibility (Panagiotidi et al., 2017). Though, these minor differences in visual processing, we found in our study may not result from early sensory processing, but from dysregulated top-down attentional processes. The performed tasks in our study need sustained attention, what is known to be regulated by dopaminergic and noradrenergic neuromodulation of the prefrontal cortex and impaired in adults with ADHD (Noudoost et al., 2010). Although rather speculative, future research is needed to disentangle the various influences of sensory processing aberrancies that lead to performance differences between people with ADHD and the neurotypical population.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The studies involving humans were approved by Kurt Racké, Ethical Committee Faculty of Medicine Bonn. The studies were conducted in accordance with the local legislation and institutional requirements. The participants provided their written informed consent to participate in this study.

MiS: formal analysis, data curation, visualization, writing, and original draft preparation, MaS: conceptualization, formal analysis, project administration, and writing, review, and editing. TG: formal analysis and writing, review, and editing. BA: recruitment and writing, review, and editing. PJ: software and paradigm realization. SL and AP: supervision and writing, review, and editing. All authors contributed to the article and approved the submitted version.

This work was supported by the Open Access Publication Fund of the University of Bonn.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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