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A neural circuit for spatial summation in visual cortex

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Abstract

The response of cortical neurons to a sensory stimulus is modulated by the context. In the visual cortex, for example, stimulation of a pyramidal cell's receptive-field surround can attenuate the cell’s response to a stimulus in the centre of its receptive field, a phenomenon called surround suppression. Whether cortical circuits contribute to surround suppression or whether the phenomenon is entirely relayed from earlier stages of visual processing is debated. Here we show that, in contrast to pyramidal cells, the response of somatostatin-expressing inhibitory neurons (SOMs) in the superficial layers of the mouse visual cortex increases with stimulation of the receptive-field surround. This difference results from the preferential excitation of SOMs by horizontal cortical axons. By perturbing the activity of SOMs, we show that these neurons contribute to pyramidal cells' surround suppression. These results establish a cortical circuit for surround suppression and attribute a particular function to a genetically defined type of inhibitory neuron.

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Figure 1: Differences in spatial summation between three types of neurons in the visual cortex.
Figure 2: SOMs are selectively excited by horizontal cortical projections.
Figure 3: Suppression of pyramidal cells by SOMs as a function of the activated layer 2/3 area.
Figure 4: SOMs contribute to size tuning of layer 2/3 pyramidal cells.

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References

  1. Allman, J., Miezin, F. & McGuinness, E. Direction- and velocity-specific responses from beyond the classical receptive field in the middle temporal visual area (MT). Perception 14, 105–126 (1985)

    Article  CAS  Google Scholar 

  2. Angelucci, A. & Bressloff, P. C. Contribution of feedforward, lateral and feedback connections to the classical receptive field center and extra-classical receptive field surround of primate V1 neurons. Prog. Brain Res. 154, 93–120 (2006)

    Article  Google Scholar 

  3. Gilbert, C. D., Das, A., Ito, M., Kapadia, M. & Westheimer, G. Spatial integration and cortical dynamics. Proc. Natl Acad. Sci. USA 93, 615–622 (1996)

    Article  ADS  CAS  Google Scholar 

  4. Hubel, D. H. & Wiesel, T. N. Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. J. Neurophysiol. 28, 229–289 (1965)

    Article  CAS  Google Scholar 

  5. Blakemore, C. & Tobin, E. A. Lateral inhibition between orientation detectors in the cat's visual cortex. Exp. Brain Res. 15, 439–440 (1972)

    Article  CAS  Google Scholar 

  6. Nelson, J. I. & Frost, B. J. Orientation-selective inhibition from beyond the classic visual receptive field. Brain Res. 139, 359–365 (1978)

    Article  CAS  Google Scholar 

  7. DeAngelis, G. C., Freeman, R. D. & Ohzawa, I. Length and width tuning of neurons in the cat's primary visual cortex. J. Neurophysiol. 71, 347–374 (1994)

    Article  CAS  Google Scholar 

  8. Knierim, J. J. & van Essen, D. C. Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. J. Neurophysiol. 67, 961–980 (1992)

    Article  CAS  Google Scholar 

  9. Levitt, J. B. & Lund, J. S. Contrast dependence of contextual effects in primate visual cortex. Nature 387, 73–76 (1997)

    Article  ADS  CAS  Google Scholar 

  10. Lamme, V. A. The neurophysiology of figure-ground segregation in primary visual cortex. J. Neurosci. 15, 1605–1615 (1995)

    Article  CAS  Google Scholar 

  11. Dobbins, A., Zucker, S. W. & Cynader, M. S. Endstopped neurons in the visual cortex as a substrate for calculating curvature. Nature 329, 438–441 (1987)

    Article  ADS  CAS  Google Scholar 

  12. Mareschal, I. & Shapley, R. M. Effects of contrast and size on orientation discrimination. Vision Res. 44, 57–67 (2004)

    Article  Google Scholar 

  13. Solomon, S. G., Lee, B. B. & Sun, H. Suppressive surrounds and contrast gain in magnocellular-pathway retinal ganglion cells of macaque. J. Neurosci. 26, 8715–8726 (2006)

    Article  CAS  Google Scholar 

  14. Alitto, H. J. & Usrey, W. M. Origin and dynamics of extraclassical suppression in the lateral geniculate nucleus of the macaque monkey. Neuron 57, 135–146 (2008)

    Article  CAS  Google Scholar 

  15. Zhang, Y., Kim, I.-J., Sanes, J. R. & Meister, M. The most numerous ganglion cell type of the mouse retina is a selective feature detector. Proc. Natl Acad. Sci. USA advance online publication, doi: 10.1073/pnas.1211547109 (13 August 2012)

  16. Murphy, P. C. & Sillito, A. M. Corticofugal feedback influences the generation of length tuning in the visual pathway. Nature 329, 727–729 (1987)

    Article  ADS  CAS  Google Scholar 

  17. Sceniak, M. P., Chatterjee, S. & Callaway, E. M. Visual spatial summation in macaque geniculocortical afferents. J. Neurophysiol. 96, 3474–3484 (2006)

    Article  Google Scholar 

  18. Bonin, V., Mante, V. & Carandini, M. The suppressive field of neurons in lateral geniculate nucleus. J. Neurosci. 25, 10844–10856 (2005)

    Article  CAS  Google Scholar 

  19. Ozeki, H. et al. Relationship between excitation and inhibition underlying size tuning and contextual response modulation in the cat primary visual cortex. J. Neurosci. 24, 1428–1438 (2004)

    Article  CAS  Google Scholar 

  20. Bolz, J. & Gilbert, C. D. Generation of end-inhibition in the visual cortex via interlaminar connections. Nature 320, 362–365 (1986)

    Article  ADS  CAS  Google Scholar 

  21. Ozeki, H., Finn, I. M., Schaffer, E. S., Miller, K. D. & Ferster, D. Inhibitory stabilization of the cortical network underlies visual surround suppression. Neuron 62, 578–592 (2009)

    Article  CAS  Google Scholar 

  22. Haider, B. et al. Synaptic and network mechanisms of sparse and reliable visual cortical activity during nonclassical receptive field stimulation. Neuron 65, 107–121 (2010)

    Article  CAS  Google Scholar 

  23. Niell, C. M. & Stryker, M. P. Highly selective receptive fields in mouse visual cortex. J. Neurosci. 28, 7520–7536 (2008)

    Article  CAS  Google Scholar 

  24. Van den Bergh, G., Zhang, B., Arckens, L. & Chino, Y. M. Receptive-field properties of V1 and V2 neurons in mice and macaque monkeys. J. Comp. Neurol. 518, 2051–2070 (2010)

    Article  Google Scholar 

  25. Margrie, T. W. et al. Targeted whole-cell recordings in the mammalian brain in vivo. Neuron 39, 911–918 (2003)

    Article  CAS  Google Scholar 

  26. Kawaguchi, Y. & Kubota, Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7, 476–486 (1997)

    Article  CAS  Google Scholar 

  27. McCormick, D. A., Connors, B. W., Lighthall, J. W. & Prince, D. A. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J. Neurophysiol. 54, 782–806 (1985)

    Article  CAS  Google Scholar 

  28. Taniguchi, H. et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71, 995–1013 (2011); erratum 72, 782–806 (2011)

    Article  Google Scholar 

  29. Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G. & Deisseroth, K. Millisecond-timescale, genetically targeted optical control of neural activity. Nature Neurosci. 8, 1263–1268 (2005)

    Article  CAS  Google Scholar 

  30. Petreanu, L., Mao, T., Sternson, S. M. & Svoboda, K. The subcellular organization of neocortical excitatory connections. Nature 457, 1142–1145 (2009)

    Article  ADS  CAS  Google Scholar 

  31. Adesnik, H. & Scanziani, M. Lateral competition for cortical space by layer-specific horizontal circuits. Nature 464, 1155–1160 (2010)

    Article  ADS  CAS  Google Scholar 

  32. Wang, Q. & Burkhalter, A. Area map of mouse visual cortex. J. Comp. Neurol. 502, 339–357 (2007)

    Article  Google Scholar 

  33. Kapfer, C., Glickfeld, L. L., Atallah, B. V. & Scanziani, M. Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nature Neurosci. 10, 743–753 (2007)

    Article  CAS  Google Scholar 

  34. Chow, B. Y. et al. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463, 98–102 (2010)

    Article  ADS  CAS  Google Scholar 

  35. Atasoy, D., Aponte, Y., Su, H. H. & Sternson, S. M. A. FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J. Neurosci. 28, 7025–7030 (2008)

    Article  CAS  Google Scholar 

  36. Ma, W. P. et al. Visual representations by cortical somatostatin inhibitory neurons–selective but with weak and delayed responses. J. Neurosci. 30, 14371–14379 (2010)

    Article  CAS  Google Scholar 

  37. Cavanaugh, J. R., Bair, W. & Movshon, J. A. Selectivity and spatial distribution of signals from the receptive field surround in macaque V1 neurons. J. Neurophysiol. 88, 2547–2556 (2002)

    Article  Google Scholar 

  38. Kapadia, M. K., Westheimer, G. & Gilbert, C. D. Dynamics of spatial summation in primary visual cortex of alert monkeys. Proc. Natl Acad. Sci. USA 96, 12073–12078 (1999)

    Article  ADS  CAS  Google Scholar 

  39. Sceniak, M. P., Ringach, D. L., Hawken, M. J. & Shapley, R. Contrast’s effect on spatial summation by macaque V1 neurons. Nature Neurosci. 2, 733–739 (1999)

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to J. Evora for the reconstruction of SOMs and technical assistance. We thank C. Niell and M. Stryker for providing expertise and sharing code used at the initial stages of this project; S. Olsen for providing the firing rates of part of the units isolated under anaesthesia; P. Abelkop and A. Linder for technical assistance; and J. Isaacson and members of the Scanziani laboratory for helpful advice. H.A. was supported by the Helen Hay Whitney Foundation and the Howard Hughes Medical Institute (HHMI). W.B. and M.S. were supported by the HHMI, the Gatsby charitable foundation and US National Institute of Health grant NS069010.

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Contributions

Author Contributions H.A. and M.S. designed the study. H.A. conducted all experiments. W.B. conducted all in vivo data analysis and spike sorting. H.T. and Z.J.H. generated the SOM-IRES-CRE mice. M.S. and H.A. wrote the paper.

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Correspondence to Massimo Scanziani.

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The authors declare no competing financial interests.

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Adesnik, H., Bruns, W., Taniguchi, H. et al. A neural circuit for spatial summation in visual cortex. Nature 490, 226–231 (2012). https://doi.org/10.1038/nature11526

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