Facilitation of temporal prediction by electrical stimulation to the primate cerebellar nuclei

Abstract

The cerebellum is known to be involved in temporal information processing. However, the underlying neuronal mechanisms remain unclear. In our previous study, monkeys were trained to make a saccade in response to a single omission of periodically presented visual stimuli. To detect stimulus omission, animals had to predict the timing of each next stimulus. During this task, neurons in the cerebellar dentate nucleus exhibited a transient decrement of activity followed by a gradual increase in firing rate that peaked around the time of the next stimulus (Ohmae et al., 2013). In the present study, to address how these two components of neuronal activity contributed to omission detection, we applied electrical microstimulation to the recording site at different timing during the task. We found that electrical stimulation just before the stimulus omission shortened the latencies of both contraversive and ipsiversive saccades. Because the changes in saccade latency non-linearly depended on the timing of stimulation in each inter-stimulus interval, and electrical stimulation just before the early stimulus in the sequence failed to evoke saccades, the neuronal activity in the dentate nucleus might regulate temporal prediction rather than facilitating saccade execution. Our results support the hypothesis that the firing modulation in each inter-stimulus interval in the dentate nucleus represents neuronal code for the temporal prediction of next stimulus. AbbreviationsFP, fixation point; MRI, magnetic resonance images; SOA, stimulus onset asynchrony

Entrained neuronal activity to periodic visual stimuli in the primate striatum compared with the cerebellum

“…We previously demonstrated that the periodic neuronal modulation in the cerebellar dentate nucleus depended on the stimulus interval, showing a greater firing modulation for longer ISIs (Ohmae et al, 2013; Uematsu et al, 2017). In this study, we also found that the magnitude of periodic activity in the caudate nucleus altered as the ISI was systematically varied from 100 to 600 ms. Like neurons in the cerebellum, a representative caudate neuron shown in Figure 4A exhibited greater firing modulation for longer ISIs.…”

“…Nevertheless, the activity of these neurons as well as behavioral parameters could be altered by systematic changes in the reward schedule. For example, the gradual rise of neuronal activity during stimulus repetition (Figure 3D), which likely reflected temporal expectation of the stimulus omission in each trial (Uematsu et al, 2017), might be scaled by the amount of reward. This possibility is to be tested in future studies.…”

“…We also demonstrated in monkeys that neurons in the cerebellar dentate nucleus during the task exhibited entrainment of activity, and that neuronal modulation for each stimulus was proportional to the inter-stimulus interval (ISI) (Ohmae et al, 2013). Because local inactivation and electrical stimulation applied to the recording sites delayed and promoted the detection of the stimulus omission, respectively, the periodic neuronal signals in the cerebellar nucleus likely contributed to the prediction of stimulus timing during the task (Ohmae and Tanaka, 2016; Ohmae et al, 2013; Uematsu et al, 2017).…”

Entrainment and maintenance of an internal metronome in supplementary motor area

“…Adaptive behavior benefits from the ability to discern temporal regularities in the environment. To exploit these regularities, the brain must be able to measure time intervals between repetitive events ( Buhusi and Meck, 2005 ; de Lafuente et al, 2015 ; Confais et al, 2012 ; Leon and Shadlen, 2003 ; Grahn and Brett, 2007 ; Merchant and Lafuente, 2014 ; Merchant et al, 2015 ), and use this timing information to anticipate future events ( Goel and Buonomano, 2014 ; Jazayeri and Shadlen, 2010 ; Uematsu et al, 2017 ). This behavior is evident when we dance to music, which requires perceiving rhythms and generating movements in sync with them ( Levitin et al, 2018 ).…”

Entrainment and maintenance of an internal metronome in premotor cortex

“…Adaptive behavior benefits from the ability to discern temporal regularities in the environment. To exploit these regularities, the brain must be able to measure time intervals between repetitive events (Buhusi and Meck 2005; de Lafuente, Jazayeri, and Shadlen 2015; Confais et al 2012; Leon and Shadlen 2003), and use this timing information to anticipate future events (Goel and Buonomano 2014; Jazayeri and Shadlen 2010; Uematsu, Ohmae, and Tanaka 2017). This behavior is evident when we dance to music, which requires perceiving rhythms and generating movements in sync with them (Levitin, Grahn, and London 2018).…”