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Entrained rhythmic activities of neuronal ensembles as perceptual memory of time interval

Abstract

The ability to process temporal information is fundamental to sensory perception, cognitive processing and motor behaviour of all living organisms, from amoebae to humans1,2,3,4. Neural circuit mechanisms based on neuronal and synaptic properties have been shown to process temporal information over the range of tens of microseconds to hundreds of milliseconds5,6,7. How neural circuits process temporal information in the range of seconds to minutes is much less understood. Studies of working memory in monkeys and rats have shown that neurons in the prefrontal cortex8,9,10, the parietal cortex9,11 and the thalamus12 exhibit ramping activities that linearly correlate with the lapse of time until the end of a specific time interval of several seconds that the animal is trained to memorize. Many organisms can also memorize the time interval of rhythmic sensory stimuli in the timescale of seconds and can coordinate motor behaviour accordingly, for example, by keeping the rhythm after exposure to the beat of music. Here we report a form of rhythmic activity among specific neuronal ensembles in the zebrafish optic tectum, which retains the memory of the time interval (in the order of seconds) of repetitive sensory stimuli for a duration of up to 20 s. After repetitive visual conditioning stimulation (CS) of zebrafish larvae, we observed rhythmic post-CS activities among specific tectal neuronal ensembles, with a regular interval that closely matched the CS. Visuomotor behaviour of the zebrafish larvae also showed regular post-CS repetitions at the entrained time interval that correlated with rhythmic neuronal ensemble activities in the tectum. Thus, rhythmic activities among specific neuronal ensembles may act as an adjustable ‘metronome’ for time intervals in the order of seconds, and serve as a mechanism for the short-term perceptual memory of rhythmic sensory experience.

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Figure 1: Visual-stimulation-evoked Ca 2+ transients in an ensemble of tectal neurons.
Figure 2: Repetitive conditioning stimulation induces post-CS rhythmic Ca 2+ transients.
Figure 3: Rhythmic activities of neuronal ensembles are stimulus-specific.
Figure 4: Repetitive visual CS induces post-CS rhythmic motor behaviour.

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Acknowledgements

We thank A. Kampff, F. Engert, Y. Fu and S. Smith for their help with two-photon microscopy, C. Niell for advice on the zebrafish preparation, N. Farchi, Y. Loewenstein, B. Hochner, G. de Polavieja and A. Noe for comments on the manuscript, and A. Arrenberg, B. Barak, V. Yoon, R. Chen and J. Sumbre for their technical help. This work was supported by the US National Institutes of Health.

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Correspondence to Mu-ming Poo.

Supplementary information

Supplementary Information

This file contains Supplementary Methods and References, and Supplementary Figures 1-9 with Legends (PDF 2362 kb)

Supplementary Movie

This file contains Supplementary Movie 1- Entrainment of rhythmic motor behaviour. The movie shows the tail of a zebrafish larva with its head (outside the movie frame) embedded in the agarose, during the last 4 conditioning stimuli of a series of 20 light flashes (ISI of 6 s) and the first two rhythmic cycles following CS. The tone indicates the onset of the stimuli and the entrained interval time (6 and 12 s) following the CS. Note that during the last two cycles of CS the larva initiated the tail movement shortly before the onset of the light stimulus, suggesting an “anticipatory” motor behaviour. (AVI 31405 kb)

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Sumbre, G., Muto, A., Baier, H. et al. Entrained rhythmic activities of neuronal ensembles as perceptual memory of time interval. Nature 456, 102–106 (2008). https://doi.org/10.1038/nature07351

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