Spontaneous and stimulus-driven rhythmic behaviors in ADHD adults and controls

Abstract

Many aspects of human behavior are inherently rhythmic, requiring production of rhythmic motor actions as well as synchronizing to rhythms in the environment. It is wellestablished that individuals with ADHD exhibit deficits in temporal estimation and timing functions, which may impact their ability to accurately produce and interact with rhythmic stimuli. In the current study we seek to understand the specific aspects of rhythmic behavior that are implicated in ADHD. We specifically ask whether they are attributed to imprecision in the internal generation of rhythms or to reduced acuity in rhythm perception. We also test key predictions of the Preferred Period Hypothesis, which suggests that both perceptual and motor rhythmic behaviors are biased towards a specific personal 'default' tempo. To this end, we tested several aspects of rhythmic behavior and the correspondence between them, including spontaneous motor tempo (SMT), preferred auditory perceptual tempo (PPT) and synchronization-continuations tapping in a broad range of rhythms, from sub-second to supra-second intervals. Moreover, we evaluate the intra-subject consistency of rhythmic preferences, as a means for testing the reality and reliability of personal 'default-rhythms'.We used a modified operational definition for assessing SMT and PPT, instructing participants to tap or calibrate the rhythms most comfortable for them to count along with, to avoid subjective interpretations of the task.Our results shed new light on the specific aspect of rhythmic deficits implicated in ADHD adults. We find that individuals with ADHD are primarily challenged in producing and maintaining isochronous self-generated motor rhythms, during both spontaneous and memory-paced tapping. However, they nonetheless exhibit good flexibility for synchronizing to a broad range of external rhythms, suggesting that auditory-motor entrainment for simple rhythms is preserved in ADHD, and that the presence of an external pacer allows overcoming their inherent difficulty in self-generating isochronous motor rhythms. In addition, both groups showed optimal memory-paced tapping for rhythms near their 'counting-based' SMT and PPT, which were slightly faster in the ADHD group. This is in line with the predictions of the Preferred Period Hypothesis, indicating that at least for this well-defined rhythmic behavior (i.e., counting), individuals tend to prefer similar time-scales in both motor production and perceptual evaluation.

Memory-paced tapping to auditory rhythms: Effects of rate, speech and motor-engagement

“…Here we studied the contribution of three factors to the human ability to synchronize with and reproduce rhythms in the environment: The role of motor engagement, the type of stimuli the rhythmic input is comprised of, and how performance varies across a broad range of rates. Consistent with previous findings, individuals displayed a large dynamic range for synchronization with near-perfect performance across all rates, with the exception of the extremely fast rhythms (SOA < 0.35 sec) (Kliger Amrani and Zion Golumbic 2020a). Similar synchronization accuracy was found for both simple tone rhythms and counting rhythms, which is indicative of the extraordinary flexibility of action-perception loops to adapt dynamically to the diverse range of rhythms in our environment (Repp and Steinman 2010; Chauvigné et al 2014; Pérez-González and Malmierca 2014; Zamm et al 2015).…”

“…These measures capture complementary aspects of tapping accuracy, as described in our previous work (Kliger Amrani and Zion Golumbic 2020b, 2020a) (Figure 2).…”

“…Previous studies have found that there is a relatively narrow range of rates for which memory-paced tapping is optimal, roughly around ~ 0.6 sec SOA (1.6 Hz). This range corresponds to the rates of spontaneous motor rhythms and perceptual auditory preferences (McAuley et al 2006; McAuley 2010; Roerdink et al 2011; Large and Gray 2015a; Scheurich et al 2018; Zamm et al 2018; Kliger Amrani and Zion Golumbic 2020b, 2020a), leading to the suggestion that they reflect physiological rhythmic-defaults of the auditory and/or motor systems. Given these presumed built-in default rhythmic preferences, here we further tested whether the potential effect of motor engagement manifests similarly across a broad range of rates (from sub-second to supra-second) or whether it interacts with presumed default rhythmic preferences.…”

“…In other words, continuation tapping is driven by auditory imagery of a previously-experienced rhythm, rather than by the rhythmic stimulus. The distinction between stimulus-driven (synchronization) and memory-paced (continuation) tapping has been shown to be critical for understanding the nature of rhythmic deficits in several clinical conditions, such as Parkinson’s and ADHD as well as some learning disabilities (Thaut et al 2001; Tierney and Kraus 2014; Woodruff Carr et al 2014; Hove et al 2017; Harrison et al 2018; Jaeger et al 2018; Kliger Amrani and Zion Golumbic 2020a).…”

“…However, it provides a well-controlled framework for assessing whether individuals can synchronize to- and form robust internal representations for speech-derived rhythms, as they can for simple isochronous rhythms. Moreover, given the above-mentioned default rhythmic-preferences observed for spontaneous motor rhythms and isochronous tones (Roerdink et al 2011; Large and Gray 2015a; Scheurich et al 2018; Zamm et al 2018; Kliger Amrani and Zion Golumbic 2020b, 2020a), this setup allows us to assess whether these defaults are present for speech-derived rhythms as well (Assaneo et al 2021). If we find that synchronization and memory-paced tapping to simple and speech-derived rhythms share similar optimal rates, this would support the existence of a common rhythmic mechanism, such as default neural oscillations, underlying a variety of ecologically-relevant rhythmic behaviors.…”