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.

Keywords: attention; basal ganglia; cerebellum; temporal predictions.

Fig. 1.

Experimental paradigm. Participants viewed a stream of flickering colored squares and detected a target (green square) by providing a speeded response (75% of the trials, Upper half). When there was no target, they were to withhold response (25% of the trials, Lower half). (Left) Rhythmic condition. Identical time interval between all stimuli. (Center) Single-interval condition. The interval between the white square (warning signal, WS) and target was the same as that between the two red squares, but the interval between the two pairs was random. (Right) Random: all intervals are randomly jittered. In all three conditions, the stimulus rate could be slow (Upper row) or fast (Lower row).

Fig. 2.

(A) Mean RTs for CD patients to the visual target, demonstrating RT benefit in the rhythmic condition but not in the single-interval condition. (B) Mean RTs for CD-matched healthy controls, demonstrating RT benefits in both predictive conditions. (C) Comparison of RT benefits in the two predictive conditions relative to the random condition between the CD and CD-matched groups, presented as the mean difference in log-transformed RTs. Positive values indicate larger benefit. CD leads to significant impairment in the single-interval condition only. (D) Mean RTs for PD patients, demonstrating RT benefit in the single-interval condition but not in the rhythmic condition. (E) Mean RTs for PD-matched healthy controls, demonstrating RT benefits in both predictive conditions. (F) Same as C for the PD vs. PD-matched groups. PD leads to significant impairment in the rhythm condition only. Bold font indicates significant difference (P < 0.05). All statistical analyses were performed after RT data had been log-transformed (Materials and Methods). The y axes in the panels of A, B, D, and E have different baseline values but span an identical range. In all panels, error bars represent SEM.