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Activity recall in a visual cortical ensemble

Nature Neuroscience volume 15, pages 449–455 (2012)Cite this article

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Abstract

Cue-triggered recall of learned temporal sequences is an important cognitive function that has been attributed to higher brain areas. Here recordings in both anesthetized and awake rats demonstrate that after repeated stimulation with a moving spot that evoked sequential firing of an ensemble of primary visual cortex (V1) neurons, just a brief flash at the starting point of the motion path was sufficient to evoke a sequential firing pattern that reproduced the activation order evoked by the moving spot. The speed of recalled spike sequences may reflect the internal dynamics of the network rather than the motion speed. In awake rats, such recall was observed during a synchronized ('quiet wakeful') brain state having large-amplitude, low-frequency local field potential (LFP) but not in a desynchronized ('active') state having low-amplitude, high-frequency LFP. Such conditioning-enhanced, cue-evoked sequential spiking of a V1 ensemble may contribute to experience-based perceptual inference in a brain state–dependent manner.

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Figure 1: Sequential spiking of neuronal ensemble in rat V1 evoked by moving spot.
Figure 2: Conditioning-induced increase of sequential spiking in anesthetized and awake rats.
Figure 3: Specificity of cue-triggered recall of spike sequence.
Figure 4: Persistence of conditioning-induced increase in sequential spiking in awake rats.
Figure 5: Dependence of sequence learning on conditioning parameters and NMDA receptor activation, measured in anesthetized rats.
Figure 6: Dependence of sequence recall on brain state in awake rats.

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Acknowledgements

We thank G. Buzsaki, H.D. Lv and H.S. Yao for comments and suggestions. This work was supported by 973 Program (2011CBA00400), SSSTC Program GJHZ0902 and the Knowledge Innovation Program of the Chinese Academy of Sciences (KSCX2-YW-R-29). Y.D. was supported in part by the Howard Hughes Medical Institute and M.-m.P. by a grant from the US National Institutes of Health (NS036999).

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Author notes

  1. Shengjin Xu and Wanchen Jiang: These authors contributed equally to this work.

Authors and Affiliations

  1. Institute of Neuroscience, State Key Laboratory of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China

    Shengjin Xu, Wanchen Jiang & Mu-ming Poo

  2. Graduate School of the Chinese Academy of Sciences, Shanghai, China

    Shengjin Xu & Wanchen Jiang

  3. Division of Neurobiology, Department of Molecular and Cell Biology, Helen Wills Institute of Neuroscience, University of California, Berkeley, California, USA

    Mu-ming Poo & Yang Dan

  4. Howard Hughes Medical Institute, University of California, Berkeley, California, USA

    Yang Dan

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Contributions

S.X. and W.J. conducted all experiments and performed all data analyses; S.X., W.J., M-m.P. and Y.D. designed the experiments and wrote the manuscript.

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Correspondence to Mu-ming Poo.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–9 (PDF 2594 kb)

Supplementary Movie 1

Awake head-fixed rat during visual stimulation. This video shows the behavior (eye movement, facial movement and whiskering) and LFP of awake head-fixed rat during testing and conditioning periods. Red circle indicates pupil size and position. Arrows point to reflections of the test stimuli (S and E, presented with an LCD monitor in front of the left eye) off the eyeball. The stationary bright spot on the left of the eye is the reflection of the infrared light source that provides illumination for the camera. Horizontal and vertical eye positions are shown in the traces below. Also shown are simultaneously recorded LFP, together with red/blue lines indicating synchronized/desynchronized brain states, and the short bars below indicating periods of visual stimulation. Note that the desynchronized brain state is associated with some facial and whisker movement. (MOV 3064 kb)

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Xu, S., Jiang, W., Poo, Mm. et al. Activity recall in a visual cortical ensemble. Nat Neurosci 15, 449–455 (2012). https://doi.org/10.1038/nn.3036

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