Temporal Generalization of Synchronized Saccades Beyond the Trained Range in Monkeys.

Ryuji Takeya,Aniruddh D Patel,Masaki Tanaka

doi:10.3389/fpsyg.2018.02172

Abstract

Synchronized movements with external periodic rhythms, such as dancing to a beat, are commonly observed in daily life. Although it has been well established that some vocal learning species (including parrots and humans) spontaneously develop this ability, it has only recently been shown that monkeys are also capable of predictive and tempo-flexible synchronization to periodic stimuli. In our previous study, monkeys were trained to make predictive saccades for alternately presented visual stimuli at fixed stimulus onset asynchronies (SOAs) to obtain a liquid reward. The monkeys generalized predictive synchronization to novel SOAs in the middle of trained range, suggesting a capacity for tempo-flexible synchronization. However, it is possible that when encountering a novel tempo, the monkeys might sample learned saccade sequences from those for the short and long SOAs so that the mean saccade interval matched the untrained SOA. To eliminate this possibility, in the current study we tested monkeys on novel SOAs outside the trained range. Animals were trained to generate synchronized eye movements for 600 and 900-ms SOAs for a few weeks, and then were tested for longer SOAs. The accuracy and precision of predictive saccades for one untrained SOA (1200 ms) were comparable to those for the trained conditions. On the other hand, the variance of predictive saccade latency and the proportion of reactive saccades increased significantly in the longer SOA conditions (1800 and 2400 ms), indicating that temporal prediction of periodic stimuli was difficult in this range, similar to previous results on synchronized tapping in humans. Our results suggest that monkeys might share similar synchronization mechanisms with humans, which can be subject to physiological examination in future studies.

Highlights

We have an advanced ability to synchronize our movements with external rhythms, such as dancing and singing to a beat, behaviors seen in every human culture (McNeil, 1997; Savage et al, 2015)
The distribution of saccade latencies centered at negative value, which was similar to the “negative asynchrony” known in synchronized tapping in humans (Engström et al, 1996; stimulus onset asynchronies (SOAs) conditions (2, 5, 12, 45, and 47%), suggesting that the animal had a difficulty in predicting the target timing when SOA was long
The animal obtained a small amount of reward for reactive saccades in the condition with longer SOAs, a significant number of predictive saccades were still observed, indicating that the animal attempted to generate synchronized saccades

Summary

Introduction

We have an advanced ability to synchronize our movements with external rhythms, such as dancing and singing to a beat, behaviors seen in every human culture (McNeil, 1997; Savage et al, 2015). Sea lions can acquire this ability with extensive training (Cook et al, 2013; Rouse et al, 2016), and chimpanzees and bonobos spontaneously show some aspects of this ability (Hattori et al, 2013; Large and Gray, 2015). Unlike monkeys these larger mammals are not suited for extensive neuronal recording and pharmacological manipulations. We found that monkeys were able to generate predictive synchronized saccades with novel tempi, suggesting that they had the capacity for predictive tempo-flexible synchronization

Methods

Results

Discussion

Conclusion