The human cerebellum is essential for modulating perceptual sensitivity based on temporal expectations
Abstract
A functional benefit of attention is to proactively enhance perceptual sensitivity in space and time. Although attentional orienting has traditionally been associated with cortico-thalamic networks, recent evidence has shown that individuals with cerebellar degeneration (CD) show a reduced reaction time benefit from cues that enable temporal anticipation. While this deficit may reflect impairment in anticipatory motor preparation, it could also arise from cerebellar contribution to attentional modulation in time of perceptual sensitivity. To examine this, we tested CD participants on a non-speeded, challenging perceptual discrimination task, asking if they benefit from temporal cues. Strikingly, the CD group showed no duration-specific perceptual sensitivity benefit when cued by repeated but aperiodic presentation of the target interval. In contrast, they performed similar to controls when cued by a rhythmic stream. This dissociation further specifies the functional domain of the cerebellum and establishes its role in the attentional adjustment of perceptual sensitivity in time.
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Reviewer #3 (Public Review):
This study investigates the temporal orientation abilities of cerebellar degeneration and control subjects during an orientation discrimination task of visual stimuli with showed a contrast near threshold. Participants were queried to express their discrimination decision with a response only after a random delay following target offset, which decreases the motor preparation component of the task in the interval-based condition. CD subjects showed similar visual discrimination performance to controls when cued by a rhythmic set of stimuli but showed no benefit when the target interval was presented aperiodically. The authors interpret these findings as evidence supporting the notion that the cerebellum plays a role in interval based attentional orienting to proactively modulate perception. This is an …
Reviewer #3 (Public Review):
This study investigates the temporal orientation abilities of cerebellar degeneration and control subjects during an orientation discrimination task of visual stimuli with showed a contrast near threshold. Participants were queried to express their discrimination decision with a response only after a random delay following target offset, which decreases the motor preparation component of the task in the interval-based condition. CD subjects showed similar visual discrimination performance to controls when cued by a rhythmic set of stimuli but showed no benefit when the target interval was presented aperiodically. The authors interpret these findings as evidence supporting the notion that the cerebellum plays a role in interval based attentional orienting to proactively modulate perception. This is an elegantly simple experiment providing a novel observation in the field.
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Reviewer #2 (Public Review):
The article by Breska and Ivry provides a nice, timely, and relevant continuation of their previous recent work on the role of the cerebellum in interval-based (but not rhythm-based) anticipation in time. While in their related prior work (in particular their recent articles in PNAS and Science Advances) the authors used simple reaction time tasks that made it difficult to attribute the observed effects to visual vs. motor anticipatory mechanisms, in the current work they used a perceptual discrimination task with a delayed response to focus on potential contributions of the cerebellum to temporal anticipation specifically for perceptual sensitivity (where the role of the cerebellum is less obvious, given it has traditionally been implicated more in motor control than in perception). They do so by comparing …
Reviewer #2 (Public Review):
The article by Breska and Ivry provides a nice, timely, and relevant continuation of their previous recent work on the role of the cerebellum in interval-based (but not rhythm-based) anticipation in time. While in their related prior work (in particular their recent articles in PNAS and Science Advances) the authors used simple reaction time tasks that made it difficult to attribute the observed effects to visual vs. motor anticipatory mechanisms, in the current work they used a perceptual discrimination task with a delayed response to focus on potential contributions of the cerebellum to temporal anticipation specifically for perceptual sensitivity (where the role of the cerebellum is less obvious, given it has traditionally been implicated more in motor control than in perception). They do so by comparing individuals with cerebellar degeneration to controls, and finding a selective impairment of the individuals with cerebellar degeneration to use interval-based temporal predictions to facilitate visual discrimination, while rhythm-based performance benefits are spared (providing a neat comparison and control).
I have no major comments to detail. The short report is well written, complements related work by the authors nicely, and makes an important and novel contribution to the literature on temporal anticipation (while also having relevant implications more generally for views on the role of the cerebellum in cognition).
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Reviewer #1 (Public Review):
Breska and Ivry tested the role of the cerebellum in temporal expectation, specifically in how temporal expectation affects perception. The question is interesting, as the neural mechanisms mediating the substantial effects of temporal expectation on perception are not well understood. The authors found that in a perceptual discrimination task, individuals with cerebellar degeneration (CD) showed reduced effects of temporal expectation on discriminability with interval timing cues, but intact effects with rhythmic cues. This shows that the role of the cerebellum in temporal expectation (which had been previously demonstrated by the authors) is not merely one of motor preparation. Rather, the cerebellum appears to play a causal role in bringing about the perceptual consequences of temporal expectation for …
Reviewer #1 (Public Review):
Breska and Ivry tested the role of the cerebellum in temporal expectation, specifically in how temporal expectation affects perception. The question is interesting, as the neural mechanisms mediating the substantial effects of temporal expectation on perception are not well understood. The authors found that in a perceptual discrimination task, individuals with cerebellar degeneration (CD) showed reduced effects of temporal expectation on discriminability with interval timing cues, but intact effects with rhythmic cues. This shows that the role of the cerebellum in temporal expectation (which had been previously demonstrated by the authors) is not merely one of motor preparation. Rather, the cerebellum appears to play a causal role in bringing about the perceptual consequences of temporal expectation for predictable intervals. It also reveals differences between interval timing and rhythmic manipulations in terms of the mechanisms by which they affect perception.
This is a straightforward study with a clean experimental approach and clear presentation of the data. However, I felt the manuscript would benefit from a more thorough analysis of the dataset, especially given the rarity of individuals with CD.
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Evaluation Summary:
This study provides evidence that individuals with cerebellar degeneration show reduced effects of temporal expectation on perceptual discriminability with interval timing cues, but intact effects with rhythmic cues. The authors compare individuals with cerebellar degeneration to controls, and find a selective impairment of the individuals with cerebellar degeneration to use interval-based temporal predictions to facilitate visual discrimination, whereas rhythm-based performance benefits are spared. This study is of interest to psychologists and neuroscientists investigating prediction, perception, attention, and motor control, as it demonstrates a key role for the cerebellum in mediating the effects of interval-based temporal expectation on perception.
(This preprint has been reviewed by eLife. We include the public …
Evaluation Summary:
This study provides evidence that individuals with cerebellar degeneration show reduced effects of temporal expectation on perceptual discriminability with interval timing cues, but intact effects with rhythmic cues. The authors compare individuals with cerebellar degeneration to controls, and find a selective impairment of the individuals with cerebellar degeneration to use interval-based temporal predictions to facilitate visual discrimination, whereas rhythm-based performance benefits are spared. This study is of interest to psychologists and neuroscientists investigating prediction, perception, attention, and motor control, as it demonstrates a key role for the cerebellum in mediating the effects of interval-based temporal expectation on perception.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)
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