Double dissociation of single-interval and rhythmic temporal prediction in cerebellar degeneration and Parkinson’s disease

Abstract

Predicting the timing of upcoming events is critical for successful interaction in a dynamic world, and is recognized as a key computation for attentional orienting. Temporal predictions can be formed when recent events define a rhythmic structure, as well as in aperiodic streams or even in isolation, when a specified interval is known from previous exposure. However, whether predictions in these two contexts are mediated by a common mechanism, or by distinct, context-dependent mechanisms, is highly controversial. Moreover, although the basal ganglia and cerebellum have been linked to temporal processing, the role of these subcortical structures in temporal orienting of attention is unclear. To address these issues, we tested individuals with cerebellar degeneration or Parkinson’s disease, with the latter serving as a model of basal ganglia dysfunction, on temporal prediction tasks in the subsecond range. The participants performed a visual detection task in which the onset of the target was predictable, based on either a rhythmic stream of stimuli, or a single interval, specified by two events that occurred within an aperiodic stream. Patients with cerebellar degeneration showed no benefit from single-interval cuing but preserved benefit from rhythm cuing, whereas patients with Parkinson’s disease showed no benefit from rhythm cuing but preserved benefit from single-interval cuing. This double dissociation provides causal evidence for functionally nonoverlapping mechanisms of rhythm- and interval-based temporal prediction for attentional orienting, and establishes the separable contributions of the cerebellum and basal ganglia to these functions, suggesting a mechanistic specialization across timing domains.

Explicit control of step timing during split-belt walking reveals interdependent recalibration of movements in space and time

“…We find that adaptation of movements to a novel walking situation results in the recalibration of internal representations for predictive control of locomotion; which are expressed as robust after-effects in temporal and spatial movement features. This is consistent with the idea that the motor system forms internal representations of space (Marigold and Drew, 2017) and time (Avraham et al, 2017; Breska and Ivry, 2018; Drew and Marigold, 2015) for predictive motor control. Several behavioral studies suggest separate recalibration of these internal representations of space and time in locomotion because spatial and timing measures exhibit different adaptation rates in the mature motor system (Malone and Bastian, 2010; Darmohray et al, 2019) throughout development (Vasudevan et al, 2011; Patrick et al, 2014) or healthy aging (Sombric et al, 2017).…”

Beat-based and memory-based temporal expectations in rhythm: similar perceptual effects, different underlying mechanisms

“…Also, beat-based and memory-based expectations to some extent interfered with each other. Similar effects on ERPs and behavior and the presence of interference may point at a shared underlying mechanism, which may be surprising given the evidence from clinical studies (Breska & Ivry, 2018) and research in nonhuman animals ) that suggests that beat-based expectations are distinct from other types of temporal expectations. Indeed, we also found evidence for distinct processing of beat-based and memory-based expectations: When the timing of events was fully predictable based on memory, the presence of beat-based expectations still deteriorated target detection and enhanced sensory responses for events off the beat (at unexpected moments), and when events were fully predictable based on the beat, memory-based expectations still improved target detection.…”

“…neural entrainment, was shown to be similarly enhanced by memory-based and beat-based expectations (Breska & Deouell, 2017b), suggesting either that phase coherence is not a good measure of entrainment, as suggested by the authors, or that entrainment is a general, rather than a context-specific, mechanism of temporal expectations (Rimmele et al, 2018). Note that in all three studies described above (Breska & Deouell, 2017b;Breska & Ivry, 2018;Morillon et al, 2016), while care was taken to design stimuli that elicited only memory-based but not beat-based expectations, responses to isochronous stimuli were used as a proxy for beat-based expectations. In addition to affording beat-based expectations, isochronous stimuli are by definition more predictable in terms of learning their intervals than any other type of memorybased sequence (e.g., only one interval needs to be learned in an isochronous sequence).…”

“…Thus, in these studies, the effects of beat-based expectations were always confounded with increases in temporal predictability based on memory. In addition, in the latter two studies (Breska & Deouell, 2017b;Breska & Ivry, 2018), static visual stimuli were used. The auditory system has repeatedly been found to be superior over the visual system in eliciting temporal expectations in humans (Grahn, 2012;Grahn, Henry, & McAuley, 2011;Zarco, Merchant, Prado, & Mendez, 2009).…”

Context-specific control of the neural dynamics of temporal attention by the human cerebellum

“…However, we have recently provided evidence that stands in contrast to a strict cortico-striatal view of temporal anticipation, showing that individuals with cerebellar degeneration (CD) failed to exhibit behavioral benefits from temporal cues on a simple detection task [28]. Importantly, the impairment was limited to conditions in which temporal anticipation was based on associations between cues and isolated intervals [6,8–10], but not when based on a periodic signal [3–7].…”