Article | Published:

Visual recognition memory, manifested as long-term habituation, requires synaptic plasticity in V1

Nature Neuroscience volume 18, pages 262271 (2015) | Download Citation

  • An Erratum to this article was published on 26 May 2015

This article has been updated

Abstract

Familiarity with stimuli that bring neither reward nor punishment, manifested through behavioral habituation, enables organisms to detect novelty and devote cognition to important elements of the environment. Here we describe in mice a form of long-term behavioral habituation to visual grating stimuli that is selective for stimulus orientation. Orientation-selective habituation (OSH) can be observed both in exploratory behavior in an open arena and in a stereotyped motor response to visual stimuli in head-restrained mice. We found that the latter behavioral response, termed a 'vidget', requires V1. Parallel electrophysiological recordings in V1 revealed that plasticity, in the form of stimulus-selective response potentiation (SRP), occurred in layer 4 of V1 as OSH developed. Local manipulations of V1 that prevented and reversed electrophysiological modifications likewise prevented and reversed memory demonstrated behaviorally. These findings suggest that a form of long-term visual recognition memory is stored via synaptic plasticity in primary sensory cortex.

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Change history

  • 09 February 2015

    In the version of this article initially published, there were quotation marks around "encoded" in the first paragraph and around "encode" in the last paragraph of the main text; these have been deleted. The second sentence of the third paragraph read "habituated in a stimulus-selective manner in V1 as SRP developed"; "in V1" has been deleted. The Figure 7d legend began "Failure of SRP induction"; the correct text is "Selective failure of SRP expression." The sixth paragraph of the Discussion began "Behavioral manifestation of the vidget required V1"; the correct text is "Behavioral expression of the vidget requires V1." The eighth paragraph of the Discussion included "first, a 'response' pathway that directly mediates the vidget and does not undergo long-term modification, and second, a 'learning' pathway"; "first," and "second," have been deleted. The errors have been corrected in the HTML and PDF versions of the article.

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Acknowledgements

We thank A. Heynen, A. Chubykin and B. Auerbach for helpful scientific discussions. We also thank E. Sklar and E. Greene-Colozzi for technical assistance, and S. Meagher for invaluable administrative support. This research was partly supported by the Howard Hughes Medical Institute, a grant from the National Eye Institute (RO1EY023037), and gifts from the Picower Institute Innovation Fund and the Picower Neurological Disorder Research Fund. We additionally acknowledge a JPB Foundation Fellowship to R.W.K., a National Institute of Mental Health training grant in support of E.S.K. (5T32MH074249) and a National Institute of Mental Health grant to J.P.G. (K99MH099654).

Author information

Affiliations

  1. The Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.

    • Sam F Cooke
    • , Robert W Komorowski
    • , Eitan S Kaplan
    • , Jeffrey P Gavornik
    •  & Mark F Bear
  2. The Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.

    • Sam F Cooke
    • , Robert W Komorowski
    • , Eitan S Kaplan
    • , Jeffrey P Gavornik
    •  & Mark F Bear
  3. Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.

    • Sam F Cooke
    • , Robert W Komorowski
    • , Eitan S Kaplan
    • , Jeffrey P Gavornik
    •  & Mark F Bear
  4. Department of Biology, Boston University, Boston, Massachusetts, USA.

    • Jeffrey P Gavornik

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Contributions

S.F.C. designed all experiments, conducted and analyzed all data from experiments described in Figures 1,2,4,6,7,8 and all Supplemental Figures, collected data shown in Figure 3, and wrote the manuscript. R.W.K. designed, conducted, analyzed and described all experiments shown in Figure 5, and participated in analysis of Figure 3. E.S.K. conducted experiments described in Figures 2 and 7. J.P.G. designed and conducted experiments in Figure 3 and developed the stimulus-generation and recording system for acquisition of data and participated in data analysis. M.F.B. designed experiments and wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Mark F Bear.

Integrated supplementary information

Supplementary information

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  1. 1.

    Supplementary Figures

    Supplementary Figures 1–10

  2. 2.

    Supplementary Methods Checklist

Videos

  1. 1.

    Orientation-selective habituation (OSH) of the vidget

    This video shows an example of an awake, head-fixed mouse with cannulae and electrodes implanted bilaterally in binocular V1. The mouse is viewing 0.05 cycles/degree, 100% contrast, phase-reversing, sinusoidal grating stimuli, as described throughout this paper (note that there are fewer phase reversals for the sake of demonstration only). The mouse is resting in a restraining tube and positioned on a piezo-electrical sensor. Visual stimuli presented to the mouse can be viewed in a mirror, which is angled so as to show the video monitor that the mouse is viewing, on the right hand side of the frame. In the first instance, an oriented grating is presented that the mouse has never seen before (novel). This stimulus elicits a typically large vidget response. Note that the mouse returns to a quiescent state almost immediately after stimulus offset. After a period of grey screen a familiar orientation that the mouse has viewed repeatedly over 8 previous days is presented. As is typical, this stimulus elicits very little behavioural response, indicative of orientation-selective habituation (OSH).

  2. 2.

    Orientation-selective habituation (OSH) in freely moving mice

    This video shows an example of a freely moving mouse in a 40 cm x 40 cm arena with video monitors positioned at either end. Note that electrodes have already been chronically implanted, bilaterally in binocular V1. The mouse explores the arena freely until a 0.05 cycles/degree, 100% contrast, phase-reversing, sinusoidal grating stimulus of an orientation that the mouse has not viewed previously (novel) is presented on one of the two monitors. This stimulus produces a typical set of behavioural responses including orienting and exploratory responses. Note that there is no evidence of an aversive response. Within this same session, after a period of grey screen presentation, a familiar orientation that the mouse has viewed repeatedly over 8 previous days appears on the same monitor. As is typical, this stimulus evokes much less behavioural response, indicative of orientation-selective habituation (OSH).

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DOI

https://doi.org/10.1038/nn.3920

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