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Cortico-cortical projections in mouse visual cortex are functionally target specific

Abstract

Neurons in primary sensory cortex have diverse response properties, whereas higher cortical areas are specialized. Specific connectivity may be important for areal specialization, particularly in the mouse, where neighboring neurons are functionally diverse. To examine whether higher visual areas receive functionally specific input from primary visual cortex (V1), we used two-photon calcium imaging to measure responses of axons from V1 arborizing in three areas with distinct spatial and temporal frequency preferences. We found that visual preferences of presynaptic boutons in each area were distinct and matched the average preferences of recipient neurons. This specificity could not be explained by organization within V1 and instead was due to both a greater density and greater response amplitude of functionally matched boutons. Projections from a single layer (layer 5) and from secondary visual cortex were also matched to their target areas. Thus, transmission of specific information to downstream targets may be a general feature of cortico-cortical communication.

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Figure 1: Functional two-photon calcium imaging from the axons of V1 projection neurons.
Figure 2: V1 axons projecting to LM, AL and PM are functionally distinct.
Figure 3: Lack of functional organization for speed in V1.
Figure 4: Layer 5 axons projecting to LM, AL and PM are functionally distinct.
Figure 5: Bias in the number of boutons with target-specific preferences.
Figure 6: Areal bias in the amplitude of responses at different speeds is explained by the activity of a small fraction of boutons.
Figure 7: Axons projecting from LM to AL and PM are functionally distinct.

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Acknowledgements

We thank A. Caiado, G. Goldey, M. Kirk, C. Mazur and D. Roumis for surgical assistance; J. Curry, A. Moffa and W. Wray for behavioral habituation of mice; S. Yurgenson for technical contributions to visual stimulation and eye-tracking software; and A. Vagodny for technical assistance. We also thank V. Berezovskii, R. Born, S. Chatterjee, M. Histed, C. Hull, A. Kerlin, W. Lee, J. Maunsell and W. Regehr for advice and discussion at all stages of the project. This work was supported by the US National Institutes of Health (R01 EY018742 and R01 EY010115) and by fellowships from the Helen Hay Whitney Foundation (L.L.G. and M.L.A.) and the Ludcke Foundation and Pierce Charitable Trust (M.L.A.).

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L.L.G. performed the experiments. L.L.G., M.L.A. and V.B. analyzed the data. V.B. built the experimental setup. L.L.G., M.L.A., V.B. and R.C.R. designed the experiments and wrote the manuscript.

Corresponding author

Correspondence to R Clay Reid.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–5 (PDF 1839 kb)

Supplementary Movie 1

Two-photon imaging of calcium transients in axonal projections. Changes in fluorescence (dF/F at 10× speed) in response to the presentation of visual stimuli (inset, 0.5× speed) for 10 individual trials. This is from the same experiment as shown in Figure 1c,d; field of view is in area PM approximately 90 μm below the surface. Range of dF/F: −0.5 to 2.5. (AVI 14409 kb)

Supplementary Movie 2

Average time course in response to visual stimuli. Time course of changes in fluorescence (dF/F at 5× speed) in response to the presentation of 9 different visual stimuli (inset, 0.5× speed) spaced at 2 octaves (1, 4 and 15 Hz at 0.02, 0.08 and 0.32 c.p.d.). The response to each stimulus is the average of 24 presentations. Same experiment as shown in Figure 1c,d. Range of dF/F: −0.15 to 0.8. (AVI 12969 kb)

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Glickfeld, L., Andermann, M., Bonin, V. et al. Cortico-cortical projections in mouse visual cortex are functionally target specific. Nat Neurosci 16, 219–226 (2013). https://doi.org/10.1038/nn.3300

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