Altered somatosensory processing in attention deficit hyperactivity disorder

doi:10.21203/rs.3.rs-3847685/v1

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Altered somatosensory processing in attention deficit hyperactivity disorder

https://doi.org/10.21203/rs.3.rs-3847685/v1

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published 13 Aug, 2024

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Background

Tactile sensitivity and sensory overload in ADHD are well-documented in clinical-, self-, and parent- reports, but empirical evidence is scarce and ambiguous and focuses primarily on children. Here, we compare both empirical and self-report tactile sensitivity and ADHD symptomatology in adults with ADHD and neurotypical controls. We evaluate whether tactile sensitivity and integration is more prevalent in ADHD and whether it is related to ADHD symptom severity.

Methods

Somatosensory evoked potential (SEP) amplitudes were measured in 27 adults with ADHD and 24 controls during four conditions (rest, stroking of the own arm, stroking of the arm by a researcher, and stroking of an object). Participants also filled out questionnaires on tactile sensitivity and ADHD symptoms and performed a Qb-test as an objective measure of ADHD symptom severity.

Results

Participants with ADHD self-reported greater tactile sensitivity and ADHD symptom severity than controls and received higher scores on the Qb-test. These values correlated with one another. ADHD participants showed lower tolerable threshold for electrical radial nerve stimulus, and greater reduction in cortical SEP amplitudes during additional tactile stimuli which was correlated with ADHD symptoms.

Conclusions

We find that ADHD symptomatology and touch sensitivity are directly linked, using both self-reports and experimental measures. We also find evidence of tactile sensory overload in ADHD, and an indication that this is linked to inattention specifically. Tactile sensitivity and sensory overload impact the functioning and life quality of many people with ADHD, and clinicians should consider this when treating their patients.

ADHD

Tactile Sensitivity

Sensory Gating

Somatosensory Processing

Attention Deficit Hyperactivity Disorder (ADHD) is characterized by inattention, hyperactivity and/or impulsivity [1]. Classified as a neurodevelopmental disorder, it is pervasive in children (5–15% globally) and about half of these diagnoses persist into adulthood [2]. Despite the prevalence of ADHD in the adult population and the significant impact it can have on an individual’s functioning, clinical and empirical research has focused mostly on children and adolescents.

Social difficulties, including understanding social information, attuning behavior to different social contexts, and reduced social contact and/or interest, are often apparent in both children and adults with ADHD. Some of these (e.g. “interrupting or intruding on others”) are included in DSM-5 diagnostic criteria [1], while others, though not diagnostic criteria, clearly emerge from observational studies (e.g., more noncompliance and/or aggression with peers [3, 4]). Rather than due to social disinterest, Nijmeijer et al [5] postulate social dysfunction in children with ADHD to be a consequence of the underlying core ADHD symptoms of hyperactivity, impulsivity, and inattention, as well as due to co-occurring psychiatric and/ or neurodevelopmental conditions common in children with ADHD such as Autism Spectrum Condition, Oppositional Defiant Disorder, and Conduct Disorder, and which are more defined by pervasive social impairments.

The sense of touch is important for social development and learning about the physical world. These developmental aspects could be affected by an altered tactile sensitivity in ADHD [6]. Sensory hypersensitivity appears to be common in ADHD: adults with ADHD report greater sensory sensitivity compared to neurotypical controls across all sensory modalities including the tactile sense [7, 8]. Touch-sensitivity affects around one in six children with ADHD [9] and parent- and clinical reports show more sensory difficulties in ADHD than in typically developing children [10, 11]. In the general population, self-reports show that more ADHD traits are associated with more sensory difficulties [12].

While sensory sensitivity in ADHD is widely discussed on popular science and self-help sites, scientific evidence on altered sensory processing is scarce and mostly relies on clinical-, self-, or parent- reports. Only a few empirical studies evaluated tactile processing in ADHD experimentally and the results are ambiguous. In children, Mangeot et al [11] show physiological abnormalities in all sensory modalities. Tactile sensitivity, specifically, shows mixed empirical results. Our previous study finds that adults with ADHD do not differ significantly from control participants with regard to thresholds for touch perception [13]. Using functional magnetic resonance imaging however, we find increased activation in somatosensory cortex to social touch, in addition to self-reported social touch aversion. Similarly, brain areas associated with sensory processing are functionally altered in ADHD [14]. A study in children finds slower reaction times and higher thresholds for tactile perception in ADHD than typically developing children – though the researchers attribute this to inattention and lower cognitive functioning [15]. One study finds that somatosensory evoked potential (SEP) amplitudes are higher in boys with ADHD than typically developing boys at the cortical but not the cervical level [16], indicating an altered higher order processing not present at the spinal cord level. Their follow-up study finds that children with co-occurrence of ADHD and Tactile Defensiveness (a pattern of hyper-sensitive responses to ordinary tactile stimulation) have highest cortical SEP amplitudes, while those with ADHD without Tactile Defensiveness have medium cortical amplitudes (though still higher amplitudes than typically developing children) [17].

Our previous magnetic resonance imaging study [13] finds, in adults with ADHD compared to control subjects, a greater activation in somatosensory cortex during skin-to-skin touch by another person and larger deactivation in insula during self-touch. Tactile sensations produced by others are considered socially relevant and are salient, whereas self-generated tactile sensations are attenuated through an efference copy [18]. The efference copy is thought to be implicated in the detection of unpredictable sensations which is important for sensing both danger and reward. Accurate and implicit distinction between self-touch and touch by others is foundational to social interactions and the development of a bodily self [19]. Furthermore, we previously found no difference in tactile detection thresholds between adults with ADHD and neurotypical adults, suggesting intact peripheral tactile processing. It remains unclear at which processing stage the signaling of tactile sensations is altered in ADHD. It further has not been investigated whether altered tactile processing is linked to symptom severity regarding hyperactivity and inattention. Therefore, our current study used somatosensory evoked potentials (SEP) in a population of adults with ADHD and age- and gender-matched neurotypical adults to expand on previous findings and explore whether such differences occur already at the spinal cord level, or whether the alterations occur more centrally. Participants performed self-touch and received touch by the experimenter on the arm during SEP recording, performed a Qb-test, an experimental, validated measure of inattention and hyperactivity, and filled in questionnaires regarding ADHD symptom severity and touch sensitivity. Given our and others’ earlier results, we hypothesized greater differences between SEP amplitudes measured during self- and other-touch in ADHD compared to neurotypical controls. We further hypothesized that SEP measures should relate to symptom severity obtained via self-reports and via Qb-test. Finally, we hypothesized greater touch sensitivity in the ADHD group as indicated by larger baseline SEP amplitudes and higher scores on the self-report tactile questionnaire.

Participants

ADHD participants (n = 27; mean age 25.2; SD 4.95; range 18–35; 16 female;) were recruited from the adult psychiatric clinic at the local hospitals and through online advertisements. Exclusion criteria included: any co-occurring current psychiatric disorder (such as, but not exclusively, psychosis, bipolar disorder, OCD), autism spectrum disorder, alcohol or substance use disorder within the past year, chronic pain, or any other major health concern. Participants refrained from taking stimulant medication for 24 hours prior to participation. Matched neurotypical participants (NT) (n = 24; mean age 25.3¸SD 4.83; range 19–35; 14 female;) were recruited from online advertisements. Exclusion criteria were assessed by a nurse during a telephone interview and included: any psychiatric disorder, alcohol or substance use disorder, chronic pain, or any other major health concern. During the visit, all participants filled in questionnaires pertaining to ADHD symptoms (ASRS, [20]), and tactile sensitivity (based on the tactile questions from the sensory perception quotient [21] and from sensory profile [22], see supplement). Scores were compared using two-sample t-tests.

Somatosensory evoked potentials

After two baseline recordings, SEPs were recorded simultaneously with three touch conditions consisting of slow, light stroking as reported previously [23]: 1.) self-touch, during which participants stroked their own left forearm with the right hand, 2.) object-touch, where participants stroked a pillow with the right hand (control condition), and 3.) other-touch, where participants were stroked on the left forearm by the experimenter. The order of conditions was randomized, and each condition was repeated twice. The area stroked on the left forearm corresponded to innervation by the radial nerve. Participants sat in a reclining seat and were asked to close their eyes, recline, and relax as much as possible to avoid muscle artifacts. A stimulating electrode was placed at the base of the thumb to stimulate the radial nerve. Stimulus intensity was individually adjusted according to the highest level tolerable for the participant. According to a standard clinical neurophysiology protocol, 300 non-painful pulses at a maximum of 100 mA (range for this sample 7.25–15.1 mA) at 1 Hz were administered, resulting in a length of approximately 3 min per condition. Recording electrodes were placed on the C6 cervical level, and on C4, Cz, and Fz scalp positions. Electrode skin impedance was always less than 8 kΩ. Data were acquired for 100 ms after each pulse using a Nicolet EDX system with an AT2 + 6 amplifier (Carefusion, Middelton, WI53562, USA), and recorded and analyzed using Synergy 20.0 (Carefusion, Middelton, WI53562, USA). Recordings were referenced to Fz and bandpass filtered (2 Hz – 2 kHz), amplifier range was 5mV and display sensitivity was 20µV per division. Waveforms were averaged over 300 pulses for each recording electrode and over the two runs per condition, and analyzed regarding amplitude (N15 cervically, N20 cortically). Baseline to peak amplitude was calculated automatically with the baseline defined as the value right before the averaged waveform and with automatically selected peaks, which were inspected individually and manually adjusted if detected incorrectly by the algorithm. Values were compared using repeated measures ANOVA.

Qb Test

The QbTest (QbTech Ltd, www.qbtech.com) uses an infrared camera and reflective headband to monitor a participant’s head movements while they perform a 20-minute button-press task, based on the continuous performance test on a computer. Participants are presented with two different shapes (circle, square), one at a time in either of two different colors (red, blue). The participant is instructed to press a button when the same shape and color appear on the screen twice in a row. The test records parameters such as commission errors, anticipatory responses, and reaction time, while the camera monitors movement time, area, and distance. The scores are compared to a standardized, sex and age matched group from the general population, then transformed and presented in the test reports as a “Q-score” with percentiles. Q-scores consist of three main parameters (QbInattention, QbActivity, QbImpulsivity) corresponding to the three main symptom domains of ADHD: inattention (measured through reaction time and omission errors), hyperactivity (measured through movements), and impulsivity (measured through reaction time and commission errors). Higher Q-scores (especially above 1.5) generally indicate more severe ADHD symptoms. In this study, we calculated a sum of Qb scores as an indicator of symptom severity.

Demographics

Participant characteristics are presented in Table 1. The ADHD group showed higher self-reported touch sensitivity than the NT control group (t = -2.59 p = 0.013, Fig. 1A), as well as higher self-report ADHD symptom severity, measured through ASRS as a total score (t = -10.29, p < .001, Fig. 1B), with subscales for inattention (t = -10.05, p < 0.001) and hyperactivity (t = -7.98, p < 0.001). ADHD also had higher Q-score sums (t = -2.18, p = 0.034, Fig. 1C). Self-report touch sensitivity correlated positively with ASRS across groups (r = 0.419, p = .009, Fig. 1D). Q-score sums also correlated with ASRS scores (r = 0.388, p = 0.013, Fig. 1E).

Table 1

Characteristics of adults with ADHD and neurotypical control (NT) participants
	NT	ADHD	p-value
age (m, SD)	25.32 (4.83)	25.19 (4.95)	0.921
sex (N, %)	f:14 (58%) m: 10 (42%)	f: 16 (59%) m: 11 (41%)	0.958
Qb sum (m, SD)	0.88 (2.12)	2.41 (2.7)	0.034
ASRS total (m, SD)	26.11 (8.99)	52.64 (8.07)	0.009
ASRS inattention (m, SD)	15.47 (5.33)	29.96 (4.24)	< 0.001
ASRS hyperactivity (m, SD)	10.79 (5.05)	22.12 (4.35)	< 0.001
Tactile sensitivity (m, SD)	45.17 (8.49)	52.42 (9.33)	0.013
m: mean; SD: standard deviation; NT: neurotypical controls; ASRS: Adult ADHD Self-Report Scale; Qb: sum of the scores from the Qb-test; p-values obtained from two sample t-tests

SEP amplitudes

When comparing baseline C4 amplitudes, though there was a trend there was no significant difference between groups (mean ADHD ± SD = 3.36 ± 1.12, mean NT ± SD = 2.81 ± 0.8, t = -1.97, p = 0.055). Stimulus intensity (individually determined based on highest tolerable level), however, was significantly higher in NT (mean ADHD ± SD = 9.74 ± 1.46, mean NT ± SD = 10.87 ± 1.85, t = 2.442, p = .018). We therefore corrected all following analyses for individual baseline amplitudes.

Repeated measures ANOVA showed a main effect of condition (F = 123.872, p < .001) as well as a group*condition interaction (F = 7.499, p < 001, Fig. 2). Post-hoc comparisons revealed group differences for the self-touch condition (mean ADHD ± SD = -0.9 ± 0.473, mean NT ± SD = -0.541 ± 0.254, t= -3.379, p = 0.001) and the other-touch condition (mean ADHD ± SD = -0.604 ± 0.327, mean NT ± SD = -0.379 ± 0.205, t = -3.076, p = 0.003), but not for the object-touch condition (mean ADHD ± SD = -0.082 ± 0.097, mean NT ± SD = -0.05 ± 0.077, t = -1.286, p = 0.204). There was an overall difference across groups between self- and other- (t = 6.31, p < .001). There were no differences between groups for the other-vs- self-conditions groups (t=-1.650, p = 0.105). No differences were found between conditions (F = 0.886, p = 0.416) or groups (F = 0.904, p = 0.408) at the cervical level.

Correlations with symptom severity

Individually adjusted stimulus intensity and self-reported touch sensitivity showed a negative correlation across groups (r = − .425, p = .004). Touch sensitivity also correlated negatively with baseline corrected C4 amplitudes for the self- (r = -0.384, p = .012) and other- (r = − .322, p = .038) conditions. And likewise, ASRS total scores correlated negatively with baseline corrected C4 amplitudes for the self- (r = -0.431, p = .003) and other- (r = -0.342, p = 0.023) conditions.

Considering our specific hypotheses that inattention and hyperactivity might be related to sensory processing alterations, we also explored correlations with subscores: ASRS inattention subscores correlated negatively with baseline corrected C4 amplitudes for the self- (r = -0.405, p = .006) and other- (r = 0.333, p = 0.026) conditions. Hyperactivity subscores correlated weakly with the amplitude during the self- (r= -0.3, p = 0.048) but not with the amplitude during the other- (r=-0.282, p = 0.064) condition.

No correlations were found between Q score sums and C4 amplitude differences for either the self- (r=-.237, p = 0.104) or other- (r=-0.24, p = 0.101) conditions.

Our study evaluated somatosensory evoked potentials in adults with ADHD and found evidence for altered integration of tactile stimuli, which was associated with self-reported symptom severity.

We found differences between adults with an ADHD diagnosis and neurotypical matched control participants regarding self-reported ADHD symptom severity, touch sensitivity, and experimental Q-score. Self-reported touch sensitivity was associated with self-reported symptom severity across groups. Differences in symptom severity and Q-scores were unsurprising given that the participants refrained from taking stimulant medication before the study. Our findings on touch sensitivity replicated previous findings of self-, clinician-, and parent-reported tactile sensitivity in ADHD (see, e.g., [6, 8, 10]). Touch sensitivity was correlated with ADHD symptom severity, indicating that the two are specifically linked, which is in line with a self-report study of 274 non-clinical adults indicating a correlation between ASRS score and sensory sensitivity (determined via the Highly Sensitive Person Scale) in the general population [12].

We found differences for both group and condition in somatosensory cortical amplitudes, with highest amplitudes overall during rest, reduced amplitudes for the social touch condition, and lowest amplitudes during self-touch (and no difference during the object-touch control condition). This replicates previous SEP results in a healthy population [23] and shows a clear distinction at the cortical level between self-produced and other-produced tactile stimuli. Contrary to our hypothesis and previous findings from other evoked potential studies, we did not find a clear difference between groups for baseline cortical amplitude (though there was a trend). However, this might have been due to the between-group difference of the individually adjusted stimulation intensity. Participants with ADHD considered the SEP stimulation more noxious compared to the neurotypical participants. Additionally, the thresholds participants considered “noxious” negatively correlated with self-reported tactile sensitivity, i.e., the more sensitive to touch a participant reported to be in the questionnaire, the lower threshold they considered tolerable. Taken together, this provides both self-report and empirical evidence for increased tactile sensitivity in ADHD and validated our touch sensitivity questionnaire.

Due to these differences in thresholds across participants, we corrected amplitudes according to participants’ baseline amplitudes. We found differences between groups for SEP amplitudes elicited by electrical pulses simultaneous with self- and other-touch: compared to the neurotypical group, the ADHD group showed a larger amplitude decrease for both touch conditions when the electrical pulse occurred on the same arm. There were no differences between groups for the object-touch condition, indicating that the differences were driven by altered integration of touch stimuli simultaneously occurring on the same arm (same dermatome), and not by either the motor component during self-touch or any additional tactile input on a different body part, such as the tactile input through the hand touching the object in the object-touch condition.

Additionally, we found that self-reported ADHD symptoms correlated with SEP amplitudes during self- and other-touch. More severe self-reported ADHD symptoms corresponded to a greater difference in amplitude between baseline and both self- and other-touch condition. These correlations were driven by the ASRS inattention subscore. A less direct but still significant correlation was observed between self-reported touch sensitivity and amplitude difference for the self-condition, while a trend was observed for the other condition.

Taken together, these findings support a relationship between altered tactile processing and ADHD symptomatology in adults. An explanation could be that the ADHD group experienced sensory overload with both the stimulus and the stroking occurring simultaneously. A combination of attention deficit and somatosensory sensitivity could make it more difficult for people with ADHD to integrate competing tactile sensations, habituating to what is irrelevant and attending to what is relevant; a process often referred to as sensory gating. However, gating, habituation, and attenuation of sensory stimuli are dissociable phenomena describing different underlying mechanisms [24]. We will therefore here refer to the overarching process as 'sensory focus’. Sensory focus, or the lack thereof, is often reported anecdotally in the clinic, with ADHD patients having trouble ignoring the seams of their socks or the tag of a shirt. Similar sensory focus difficulties in ADHD have been described also in the auditory domain (with, for example, patients showing sensitivity “towards sounds which are unheard by others such as the humming of a refrigerator, a clock ticking, or fans” [10]). Evoked potential studies indicate an effect of auditory sensory focus capacity on attention and executive function in adults with ADHD [25]. Studies on tactile sensory focus in ADHD are inconclusive. While some results indicate enhanced habituation, others show reduced habituation, and given the limited methods employed (mainly skin conductance and heart rate) the results are difficult to interpret [26]. Given that the amplitude differences in our study correlated strongly with the ASRS inattention subscore, and less strongly but still significantly with touch sensitivity scores, sensory focus difficulties seem to be a valid explanation for our results.

We observed no differences in cervical amplitudes for any condition or between groups, indicating that the altered touch processing we observed is a cortical process. This is in line with a previous study on children with ADHD showing higher cortical amplitudes than typically developing controls but no difference cervically [16]. It also aligns with results from our previous study on adults with ADHD showing intact detection thresholds, as evidence of a more central and higher order alteration of touch perception.

The participants with ADHD in our study were young adults with no psychiatric comorbidities, who were able to independently schedule and attend the appointment while remembering to abstain from their medication for 24 hours. This arguably excludes a large subset of the ADHD population, given the high comorbidity of ADHD with other neuropsychiatric conditions and the difficulties adults with severe ADHD typically have planning and keeping appointments [27] limiting generalizability of our findings to the more severe end of the ADHD spectrum with multiple comorbidities. Since touch sensitivity correlated with symptoms severity and more specifically inattention measures, it may be speculated that individuals with more severe ADHD could also experience more issues with touch sensitivity and with being distracted or overwhelmed by touch (and other) sensory input. It is also possible that at least some of these issues may be alleviated by adequate medication, however the effects of medication on sensory focus or touch sensitivity have not been studied. Earlier studies on sensory gating mainly in the auditory modalities provided contradictory results [28, 29].

Our study found a link between ADHD symptomatology and touch sensitivity, using both self-reports and experimental measures. Adults with ADHD had lower tolerance to radial nerve stimulation in addition to greater self-reported tactile sensitivity, and these values were associated with one another. Both self-report and experimentally measured touch sensitivity correlated with self-reported overall ADHD symptom severity. Using SEPs, we found that adults with ADHD showed greater differences in cortical amplitudes relative to baseline compared to a neurotypical control group during both a self-touch condition and touch by another. This could be due to increased sensory load, as indicated by correlations between amplitude differences and both touch sensitivity and self-reported ADHD symptoms. A limitation of our study design is that the association between tactile sensitivity, SEP amplitudes, and overall ADHD symptomatology can only be investigated correlationally. It is therefore not possible to draw conclusions regarding the directionality of this association. Inattention and hyperactivity could contribute to the larger interaction of SEP amplitudes with additional touch stimulation. However, one might also speculate that increased sensitivity to tactile stimuli could lead to inattention and hyperactivity. Future studies should try to understand directionality to develop novel treatment options and better support for people in need. Independent of the mechanistic understanding of directionality, increased touch sensitivity and difficulty integrating tactile sensations may contribute to the day-to-day difficulties that individuals with ADHD experience. Clinicians need to be aware of and help their patients address potential difficulties this may incur.

Ethics approval and consent to participate

The study was performed with full signed consent of each participant and approved by the Swedish Ethical Review Authority (2016-360-31, 2017-320-32, 2020-03015).

Consent for publication

(Not applicable)

Availability of data and materials

The dataset used and analyzed during the current study are available in the supplementary materials.

Competing interests

AJC has received consultancy and speakers’ fees from Indivior, Camurus and DNE Pharma all outside the scope of this work. All other authors have no competing interests to declare.

Funding

This research was funded by a Swedish research council grant to RB (2019-01873).

Authors' contributions

MFK collected and analyzed all data and wrote the original manuscript draft. AJC and RB provided project supervision. HO and RB provided funding and resources for data collection. All authors conceptualized the study and its design, and edited and approved the final manuscript.

Acknowledgements

We would like to thank Dorota Persson for her help with SEP data collection, and Lotta Meddling for her help with data entry.

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Competing interest reported. AJC has received consultancy and speakers’ fees from Indivior, Camurus and DNE Pharma all outside the scope of this work. All other authors have no competing interests to declare.

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Altered somatosensory processing in attention deficit hyperactivity disorder

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