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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Gibbon, J., Malapani, C., Dale, C. L. & Gallistel, C. R. Toward a neurobiology of temporal cognition: Advances and challenges. Curr. Opin. Neurobiol. 7, 170–184 (1997)
Buhusi, C. V. & Meck, W. H. What makes us tick? Functional and neural mechanisms of interval timing. Nature Rev. Neurosci. 6, 755–765 (2005)
Buonomano, D. V. The biology of time across different scales. Nature Chem. Biol. 3, 594–597 (2007)
Saigusa, T., Tero, A., Nakagaki, T. & Kuramoto, Y. Amoebae anticipate periodic events. Phys. Rev. Lett. 100, 018101 (2008)
Carr, C. E. Processing of temporal information in the brain. Annu. Rev. Neurosci. 16, 223–243 (1993)
Buonomano, D. V. Timing of neural responses in cortical organotypic slices. Proc. Natl Acad. Sci. USA 100, 4897–4902 (2003)
Buonomano, D. V. & Karmarkar, U. R. How do we tell time? Neuroscientist 8, 42–51 (2002)
Rainer, G., Rao, S. C. & Miller, E. K. Prospective coding for objects in primate prefrontal cortex. J. Neurosci. 19, 5493–5505 (1999)
Quintana, J. & Fuster, J. M. From perception to action: temporal integrative functions of prefrontal and parietal neurons. Cereb. Cortex 9, 213–221 (1999)
Brody, C. D., Hernandez, A., Zainos, A. & Romo, R. Timing and neural encoding of somatosensory parametric working memory in macaque prefrontal cortex. Cereb. Cortex 13, 1196–1207 (2003)
Leon, M. I. & Shadlen, M. N. Representation of time by neurons in the posterior parietal cortex of the macaque. Neuron 38, 317–327 (2003)
Komura, Y. et al. Retrospective and prospective coding for predicted reward in the sensory thalamus. Nature 412, 546–549 (2001)
Meek, J. Functional anatomy of the tectum mesencephali of the goldfish. An explorative analysis of the functional implications of the laminar structural organization of the tectum. Brain Res. 287, 247–297 (1983)
Vanegas, H. & Ito, H. Morphological aspects of the teleostean visual system: a review. Brain Res. 287, 117–137 (1983)
Denk, W., Strickler, J. H. & Webb, W. W. Two-photon laser scanning fluorescence microscopy. Science 248, 73–76 (1990)
Stosiek, C., Garaschuk, O., Holthoff, K. & Konnerth, A. In vivo two-photon calcium imaging of neuronal networks. Proc. Natl Acad. Sci. USA 100, 7319–7324 (2003)
Niell, C. M. & Smith, S. J. Functional imaging reveals rapid development of visual response properties in the zebrafish tectum. Neuron 45, 941–951 (2005)
McLean, D. L., Fan, J., Higashijima, S., Hale, M. E. & Fetcho, J. R. A topographic map of recruitment in spinal cord. Nature 446, 71–75 (2007)
Ramdya, P., Reiter, B. & Engert, F. Reverse correlation of rapid calcium signals in the zebrafish optic tectum in vivo . J. Neurosci. Methods 157, 230–237 (2006)
Yaksi, E. & Friedrich, R. W. Reconstruction of firing rate changes across neuronal populations by temporally deconvolved Ca2+ imaging. Nature Methods 3, 377–383 (2006)
Nakai, J., Ohkura, M. & Imoto, K. A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein. Nature Biotechnol. 19, 137–141 (2001)
Gahtan, E., Tanger, P. & Baier, H. Visual prey capture in larval zebrafish is controlled by identified reticulospinal neurons downstream of the tectum. J. Neurosci. 25, 9294–9303 (2005)
Sato, T., Hamaoka, T., Aizawa, H., Hosoya, T. & Okamoto, H. Genetic single-cell mosaic analysis implicates ephrinB2 reverse signaling in projections from the posterior tectum to the hindbrain in zebrafish. J. Neurosci. 27, 5271–5279 (2007)
Bullock, T. H., Hofmann, M. H., New, J. G. & Nahm, F. K. Dynamic properties of visual evoked potentials in the tectum of cartilaginous and bony fishes, with neuroethological implications. J. Exp. Zool. 256, 142–155 (1990)
Bullock, T. H., Hofmann, M. H., Nahm, F. K., New, J. G. & Prechtl, J. C. Event-related potentials in the retina and optic tectum of fish. J. Neurophysiol. 64, 903–914 (1990)
Bullock, T. H., Karamursel, S. & Hofmann, M. H. Interval-specific event related potentials to omitted stimuli in the electrosensory pathway in elasmobranchs: an elementary form of expectation. J. Comp. Physiol. [A] 172, 501–510 (1993)
Bullock, T. H., Karamursel, S., Achimowicz, J. Z., McClune, M. C. & Basar-Eroglu, C. Dynamic properties of human visual evoked and omitted stimulus potentials. Electroencephalogr. Clin. Neurophysiol. 91, 42–53 (1994)
Schwartz, G., Harris, R., Shrom, D. & Berry, M. J. Detection and prediction of periodic patterns by the retina. Nature Neurosci. 10, 552–554 (2007)
Lister, J. A., Robertson, C. P., Lepage, T., Johnson, S. L. & Raible, D. W. nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development 126, 3757–3767 (1999)
O’Malley, D. M. et al. Optical physiology and locomotor behaviors of wild-type and nacre zebrafish. Methods Cell Biol. 76, 261–284 (2004)
Westerfield, M. The Zebrafish Book; A Guide for the Laboratory Use of Zebrafish (Danio rerio) (Eugene, Univ. Oregon Press, 2000)
Brustein, E., Marandi, N., Kovalchuk, Y., Drapeau, P. & Konnerth, A. “In vivo” monitoring of neuronal network activity in zebrafish by two-photon Ca2+ imaging. Pflugers Arch. 446, 766–773 (2003)
Brainard, D. H. The psychophysics toolbox. Spat. Vis. 10, 433–436 (1997)
Pelli, D. G. The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat. Vis. 10, 437–442 (1997)
Easter, S. S. & Nicola, G. N. The development of vision in the zebrafish (Danio rerio). Dev. Biol. 180, 646–663 (1996)
Thévenaz, P., Ruttimann, U. E. & Unser, M. A pyramid approach to subpixel registration based on intensity. IEEE Trans. Image Process. 7, 27–41 (1998)
Ritter, D. A., Bhatt, D. H. & Fetcho, J. R. In vivo imaging of zebrafish reveals differences in the spinal networks for escape and swimming movements. J. Neurosci. 21, 8956–8965 (2001)
Burgess, H. A. & Granato, M. Modulation of locomotor activity in larval zebrafish during light adaptation. J. Exp. Biol. 210, 2526–2539 (2007)
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.
Author information
Authors and Affiliations
Corresponding author
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)
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature07351
This article is cited by
-
Influence of Recent Trial History on Interval Timing
Neuroscience Bulletin (2023)
-
Zebrafish capable of generating future state prediction error show improved active avoidance behavior in virtual reality
Nature Communications (2021)
-
Velocity storage mechanism drives a cerebellar clock for predictive eye velocity control
Scientific Reports (2020)
-
Frequency selectivity of echo responses in the mouse primary auditory cortex
Scientific Reports (2018)
-
Intensify3D: Normalizing signal intensity in large heterogenic image stacks
Scientific Reports (2018)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.