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.
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
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)
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)
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)
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)
Blakemore, C. & Tobin, E. A. Lateral inhibition between orientation detectors in the cat's visual cortex. Exp. Brain Res. 15, 439–440 (1972)
Nelson, J. I. & Frost, B. J. Orientation-selective inhibition from beyond the classic visual receptive field. Brain Res. 139, 359–365 (1978)
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)
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)
Levitt, J. B. & Lund, J. S. Contrast dependence of contextual effects in primate visual cortex. Nature 387, 73–76 (1997)
Lamme, V. A. The neurophysiology of figure-ground segregation in primary visual cortex. J. Neurosci. 15, 1605–1615 (1995)
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)
Mareschal, I. & Shapley, R. M. Effects of contrast and size on orientation discrimination. Vision Res. 44, 57–67 (2004)
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)
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)
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)
Murphy, P. C. & Sillito, A. M. Corticofugal feedback influences the generation of length tuning in the visual pathway. Nature 329, 727–729 (1987)
Sceniak, M. P., Chatterjee, S. & Callaway, E. M. Visual spatial summation in macaque geniculocortical afferents. J. Neurophysiol. 96, 3474–3484 (2006)
Bonin, V., Mante, V. & Carandini, M. The suppressive field of neurons in lateral geniculate nucleus. J. Neurosci. 25, 10844–10856 (2005)
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)
Bolz, J. & Gilbert, C. D. Generation of end-inhibition in the visual cortex via interlaminar connections. Nature 320, 362–365 (1986)
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)
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)
Niell, C. M. & Stryker, M. P. Highly selective receptive fields in mouse visual cortex. J. Neurosci. 28, 7520–7536 (2008)
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)
Margrie, T. W. et al. Targeted whole-cell recordings in the mammalian brain in vivo. Neuron 39, 911–918 (2003)
Kawaguchi, Y. & Kubota, Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7, 476–486 (1997)
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)
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)
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)
Petreanu, L., Mao, T., Sternson, S. M. & Svoboda, K. The subcellular organization of neocortical excitatory connections. Nature 457, 1142–1145 (2009)
Adesnik, H. & Scanziani, M. Lateral competition for cortical space by layer-specific horizontal circuits. Nature 464, 1155–1160 (2010)
Wang, Q. & Burkhalter, A. Area map of mouse visual cortex. J. Comp. Neurol. 502, 339–357 (2007)
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)
Chow, B. Y. et al. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463, 98–102 (2010)
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)
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)
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)
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)
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)
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.
Author information
Authors and Affiliations
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.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
This file contains Supplementary Methods, additional references and Supplementary Figures 1-8. (PDF 920 kb)
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature11526
This article is cited by
-
The logic of recurrent circuits in the primary visual cortex
Nature Neuroscience (2024)
-
Local field potentials, spiking activity, and receptive fields in human visual cortex
Science China Life Sciences (2024)
-
A frontal transcallosal inhibition loop mediates interhemispheric balance in visuospatial processing
Nature Communications (2023)
-
Parvalbumin neurons enhance temporal coding and reduce cortical noise in complex auditory scenes
Communications Biology (2023)
-
A cell-type-specific error-correction signal in the posterior parietal cortex
Nature (2023)
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.