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Locomotion Controls Spatial Integration in Mouse Visual Cortex

2013; Elsevier BV; Volume: 23; Issue: 10 Linguagem: Inglês

10.1016/j.cub.2013.04.012

1879-0445

Aslı Ayaz, Aman B. Saleem, Marieke L. Schölvinck, Matteo Carandini,

Tactile and Sensory Interactions

Growing evidence indicates that responses in sensory cortex are modulated by factors beyond direct sensory stimulation [1Ghazanfar A.A. Schroeder C.E. Is neocortex essentially multisensory?.Trends Cogn. Sci. 2006; 10: 278-285Abstract Full Text Full Text PDF PubMed Scopus (991) Google Scholar, 2Matyas F. Sreenivasan V. Marbach F. Wacongne C. Barsy B. Mateo C. Aronoff R. Petersen C.C. Motor control by sensory cortex.Science. 2010; 330: 1240-1243Crossref PubMed Scopus (269) Google Scholar, 3Shuler M.G. Bear M.F. Reward timing in the primary visual cortex.Science. 2006; 311: 1606-1609Crossref PubMed Scopus (417) Google Scholar, 4Reynolds J.H. Heeger D.J. The normalization model of attention.Neuron. 2009; 61: 168-185Abstract Full Text Full Text PDF PubMed Scopus (872) Google Scholar, 5Roberts M. Delicato L.S. Herrero J. Gieselmann M.A. Thiele A. Attention alters spatial integration in macaque V1 in an eccentricity-dependent manner.Nat. Neurosci. 2007; 10: 1483-1491Crossref PubMed Scopus (99) Google Scholar, 6Harris K.D. Thiele A. Cortical state and attention.Nat. Rev. Neurosci. 2011; 12: 509-523Crossref PubMed Scopus (524) Google Scholar, 7Wörgötter F. Eysel U.T. Context, state and the receptive fields of striatal cortex cells.Trends Neurosci. 2000; 23: 497-503Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar, 8Goard M. Dan Y. Basal forebrain activation enhances cortical coding of natural scenes.Nat. Neurosci. 2009; 12: 1444-1449Crossref PubMed Scopus (398) Google Scholar]. In primary visual cortex (V1), for instance, responses increase with locomotion [9Niell C.M. Stryker M.P. Modulation of visual responses by behavioral state in mouse visual cortex.Neuron. 2010; 65: 472-479Abstract Full Text Full Text PDF PubMed Scopus (808) Google Scholar, 10Keller G.B. Bonhoeffer T. Hübener M. Sensorimotor mismatch signals in primary visual cortex of the behaving mouse.Neuron. 2012; 74: 809-815Abstract Full Text Full Text PDF PubMed Scopus (313) Google Scholar]. Here we show that this increase is accompanied by a profound change in spatial integration. We recorded from V1 neurons in head-fixed mice placed on a spherical treadmill. We characterized spatial integration and found that the responses of most neurons were suppressed by large stimuli. As in primates [11Kapadia M.K. Westheimer G. Gilbert C.D. Dynamics of spatial summation in primary visual cortex of alert monkeys.Proc. Natl. Acad. Sci. USA. 1999; 96: 12073-12078Crossref PubMed Scopus (259) Google Scholar, 12Sceniak M.P. Ringach D.L. Hawken M.J. Shapley R. Contrast’s effect on spatial summation by macaque V1 neurons.Nat. Neurosci. 1999; 2: 733-739Crossref PubMed Scopus (479) Google Scholar], this surround suppression increased with stimulus contrast. These effects were captured by a divisive normalization model [13Cavanaugh J.R. Bair W. Movshon J.A. Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons.J. Neurophysiol. 2002; 88: 2530-2546Crossref PubMed Scopus (571) Google Scholar, 14Carandini M. Heeger D.J. Normalization as a canonical neural computation.Nat. Rev. Neurosci. 2012; 13: 51-62Crossref Scopus (429) Google Scholar], where the numerator originates from a central region driving the neuron and the denominator originates from a larger suppressive field. We then studied the effects of locomotion and found that it markedly reduced surround suppression, allowing V1 neurons to integrate over larger regions of visual space. Locomotion had two main effects: it increased spontaneous activity, and it weakened the suppressive signals mediating normalization, relative to the driving signals. We conclude that a fundamental aspect of visual processing, spatial integration, is controlled by an apparently unrelated factor, locomotion. This control might operate through the mechanisms that are in place to deliver surround suppression.