Temporal Prediction Signals for Periodic Sensory Events in the Primate Central Thalamus

Abstract

Prediction of periodic event timing is an important function for everyday activities, while the exact neural mechanism remains unclear. Previous studies in nonhuman primates have demonstrated that neurons in the cerebellar dentate nucleus and those in the caudate nucleus exhibit periodic firing modulation when the animals attempt to detect a single omission of isochronous repetitive audiovisual stimuli. To understand how these subcortical signals are sent and processed through the thalamocortical pathways, we examined single-neuron activities in the central thalamus of two macaque monkeys (one female and one male). We found that three types of neurons responded to each stimulus in the sequence in the absence of movements. Reactive-type neurons showed sensory adaptation and gradually waned the transient response to each stimulus. Predictive-type neurons steadily increased the magnitude of the suppressive response, similar to neurons previously reported in the cerebellum. Switch-type neurons initially showed a transient response, but after several cycles, the direction of firing modulation reversed and the activity decreased for each repetitive stimulus. The time course of Switch-type activity was well explained by the weighted sum of activities of the other types of neurons. Furthermore, for only Switch-type neurons the activity just before stimulus omission significantly correlated with behavioral latency, indicating that this type of neuron may carry a more advanced signal in the system detecting stimulus omission. These results suggest that the central thalamus may transmit integrated signals to the cerebral cortex for temporal information processing, which are necessary to accurately predict rhythmic event timing.

The Central Thalamus: Gatekeeper or Processing Hub?

“…The results of the study by Matsuyama and Tanaka (2021) demonstrate that, in addition to their established role in regulating information flow to cortex, thalamic nuclei might actively integrate incoming signals. This fits well with previous results from studies of thalamic nuclei that border the central thalamus in both primates and rodents.…”

“…A recent study by Matsuyama and Tanaka (2021) furthers the ongoing debate about whether thalamus processes information. The authors investigated signals within the central thalamus, which comprises the caudal part of the ventral lateral thalamic nucleus (VLc), the lateral MD (MDl), and the centrolateral thalamic nucleus (CL).…”

“…In the driver/modulator framework, the thalamus gates (Zhou et al, 2020). Responses may drive the activity of reactive-type neurons reported by Matsuyama and Tanaka (2021) in central thalamus. In striatum and cerebellum, responses to each stimulus in an oddball paradigm are suppressive and occur at the time of stimulus onset (Kameda et al, 2019;Ohmae et al, 2013).…”

“…In striatum and cerebellum, responses to each stimulus in an oddball paradigm are suppressive and occur at the time of stimulus onset (Kameda et al, 2019;Ohmae et al, 2013). These responses might form the main input to predictive-type neurons observed in central thalamus (Matsuyama and Tanaka, 2021). The responses of switch-type neurons in central thalamus might result from the integration of signals observed in reactive-and predictive-type neurons (Matsuyama and Tanaka, 2021).…”

“…These responses might form the main input to predictive-type neurons observed in central thalamus (Matsuyama and Tanaka, 2021). The responses of switch-type neurons in central thalamus might result from the integration of signals observed in reactive-and predictive-type neurons (Matsuyama and Tanaka, 2021). FEF = frontal eye field; MDl = lateral MD; CL = centrolateral thalamic nucleus; VL = ventral lateral thalamic nucleus; SNr = substantia nigra reticulata; GPi = globus pallidus internal.…”