A low-level perceptual correlate of behavioral and clinical deficits in ADHD

Abstract

In many studies of attention-deficit hyperactivity disorder (ADHD), stimulus encoding and processing (perceptual function) and response selection (executive function) have been intertwined. To dissociate these functions, we introduced a task that parametrically varied low-level stimulus features (orientation and color) for fine-grained analysis of perceptual function, and that also required participants to switch their attention between feature dimensions on a trial-by-trial basis, thus taxing executive processes. Our response paradigm captured task-irrelevant motor output (TIMO), reflecting failures to use the correct stimulus-response rule. ADHD patients had substantially worse perceptual function than Controls, especially for orientation. ADHD participants had also higher TIMO; this measure was strongly affected by the switch manipulation. Across participants, the perceptual variability parameter was correlated with TIMO, suggesting that perceptual deficits could underlie executive function deficits. Based on perceptual variability alone, we were able to classify participants into ADHD and Controls with a mean accuracy of about 77%. Participants' self-reported General Executive Composite score correlated not only with TIMO but also with the perceptual variability parameter. Our results highlight the role of perceptual deficits in ADHD and the usefulness of computational modeling of behavior in dissociating perceptual from executive processes.In Attention Deficit Hyperactivity Disorder (ADHD), self-reported behavioral deficits have been attributed to differences in executive function, attention, and perceptual function. These brain functions can be objectively quantified with behavioral paradigms, but the individual components are often not well separated. ADHD patients tend to have worse executive function than Controls according to several metrics [1][2][3][4], predominantly in response execution and inhibition [5][6][7], but also in switching between stimulus-response rules [8][9][10][11]. It has been pointed out that non-executive processes, such as alertness, accumulation of evidence or drift rate, motivation, or reward processing, might interact with executive ones [12][13][14][15][16]. In the realm of visual attention, differences in accuracy or reaction time have been found in some visual search tasks but not in others [17,18], and no consistent deficits have been found in visuo-spatial orienting [19][20][21][22]. Despite evidence of impaired perceptual function in ADHD from psychiatric assessments [23,24], behavioral studies that examined the quality of perceptual encoding in ADHD in the absence of executive or attentional involvement found small and inconsistent differences (see [25] for a review). There have been attempts to dissociate executive from perceptual function in ADHD within a single task, but the results have been mixed [26][27][28][29]. One complicating factor could be that commonly used stimuli such as faces, letters, or numbers are high-dimensional and have content at many levels. Anot...

Lapses in perceptual decisions reflect exploration

“…By encouraging subjects to sample multiple options, exploration can potentially improve subjects’ knowledge of the rules of the task, helping them to increase future payoff, thus maximizing expected utility over a long period of time. This offers an explanation for the higher rate of lapses seen in humans on tasks with abstract (Raposo, Sheppard, et al, 2012), non-intuitive (Mihali et al, 2018) or non-verbalizable (Flesch et al, 2018) stimulus-response contingencies.…”

“…Dopaminergic genes have been shown to predict individual differences in uncertainty-guided exploration in humans (Frank et al, 2009), and dopaminergic disorders such as Parkinson’s disease have been shown to disrupt the uncertainty-dependence of lapses across conditions on a multisensory task (Bertolini et al, 2015). Patients with ADHD, another disorder associated with dopaminergic dysfunction, have been shown to display both increased perceptual variability and increased task-irrelevant motor output, a measure that correlates with lapses (Mihali et al, 2018). A promising avenue for future studies is to leverage the informativeness of lapses and the precise control of uncertainty afforded by multisensory tasks, in conjunction with perturbations or recordings of dopaminergic circuitry, to further elucidate the connections between perceptual and value-based decision making systems.…”

“…For instance, many of these explanations predict that lapses should occur at a constant rate, while in reality, lapses are known to reduce in frequency with training in non-human primates (Law and Gold, 2009; Cloherty et al, 2019). Further, they can occur with different frequencies for different stimuli even within the same subject (in rodents, Nikbakht et al, 2018; and humans, Mihali et al, 2018; Bertolini et al, 2015; Flesch et al, 2018), suggesting that they may reflect task-specific, associative processes that can vary within a subject.…”

A Low-Level Perceptual Correlate of Behavioral and Clinical Deficits in ADHD

“…We recruited all participants through local advertisements, including flyers and newspaper and radio advertisements. Information on the participants is presented in Mihali, Young, Adler, Halassa, and Ma ( 2018 , appendix). Participants in both groups were matched as much as possible by age, sex, and education (see Mihali et al, 2018 , Appendix, Table A1).…”

“…Information on the participants is presented in Mihali, Young, Adler, Halassa, and Ma ( 2018 , appendix). Participants in both groups were matched as much as possible by age, sex, and education (see Mihali et al, 2018 , Appendix, Table A1). Twenty ADHD participants (12 female) of mean age 35.3 ( SD 10.0, range 21 to 55) and 20 control participants (11 female) of mean age 32.5 ( SD 6.1, range 19 to 44), with no statistical difference between their ages (Wilcoxon rank-sum test, p = 0.78), participated.…”