Attention can selectively enhance neuronal responses and exclude external noise, but the neuronal computations that underlie these effects remain unknown. At the neuronal level, noise exclusion might result in altered spatial integration properties. We tested this proposal by recording neuronal activity and length tuning in neurons of the primary visual cortex of the macaque when attention was directed toward or away from stimuli presented in each neuron's classical receptive field. For cells with central-parafoveal receptive fields, attention reduced spatial integration, as demonstrated by a reduction in preferred stimulus length and in the size of the spatial summation area. Conversely, in cells that represented more peripheral locations, attention increased spatial integration by increasing the cell's summation area. This previously unknown dichotomy between central and peripheral vision could support accurate analysis of attended foveal objects and target selection for impending eye movements to peripheral objects.
Subscribe to Journal
Get full journal access for 1 year
only $4.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Haenny, P.E. & Schiller, P.H. State dependent activity in monkey visual cortex. I Single cell activity in V1 and V4 on visual tasks. Exp. Brain Res. 69, 225–244 (1988).
Luck, S.J., Chelazzi, L., Hillyard, S.A. & Desimone, R. Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. J. Neurophysiol. 77, 24–42 (1997).
Roelfsema, P.R., Lamme, V.A. & Spekreijse, H. Object-based attention in the primary visual cortex of the macaque monkey. Nature 395, 376–381 (1998).
Spitzer, H., Desimone, R. & Moran, J. Increased attention enhances both behavioral and neuronal performance. Science 240, 338–340 (1988).
Treue, S. & Maunsell, J.H.R. Attentional modulation of visual motion processing in cortical areas MT and MST. Nature 382, 539–541 (1996).
Lu, Z.L., Lesmes, L.A. & Dosher, B.A. Spatial attention excludes external noise at the target location. J. Vis. 2, 312–323 (2002).
Yeshurun, Y. & Carrasco, M. Attention improves or impairs visual performance by enhancing spatial resolution. Nature 396, 72–75 (1998).
Treue, S. & Martinez-Trujillo, J.C. Feature-based attention influences motion processing gain in macaque visual cortex. Nature 399, 575–579 (1999).
McAdams, C.J. & Maunsell, J.H.R. Effects of attention on orientation-tuning functions of single neurons in macaque cortical area V4. J. Neurosci. 19, 431–441 (1999).
Reynolds, J.H., Chelazzi, L. & Desimone, R. Competitive mechanisms subserve attention in macaque areas V2 and V4. J. Neurosci. 19, 1736–1753 (1999).
Reynolds, J.H., Pasternak, T. & Desimone, R. Attention increases sensitivity of V4 neurons. Neuron 26, 703–714 (2000).
Womelsdorf, T., Anton-Erxleben, K., Pieper, F. & Treue, S. Dynamic shifts of visual receptive fields in cortical area MT by spatial attention. Nat. Neurosci. 9, 1156–1160 (2006).
Zenger, B., Braun, J. & Koch, C. Attentional effects on contrast detection in the presence of surround masks. Vision Res. 40, 3717–3724 (2000).
Ito, M., Westheimer, G. & Gilbert, C.D. Attention and perceptual learning modulate contextual influences on visual perception. Neuron 20, 1191–1197 (1998).
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).
Angelucci, A., Levitt, J.B. & Lund, J.S. Anatomical origins of the classical receptive field and modulatory surround field of single neurons in macaque visual cortical area V1. Prog. Brain Res. 136, 373–388 (2002).
Sceniak, M.P., Ringach, D.L., Hawken, M.J. & Shapley, R. Contrast's effect on spatial summation by macaque V1 neurons. Nat. Neurosci. 2, 733–739 (1999).
Carandini, M., Heeger, D.J. & Movshon, J.A. Linearity and normalization in simple cells of the macaque primary visual cortex. J. Neurosci. 17, 8621–8644 (1997).
Thiele, A., Distler, C. & Hoffmann, K.P. Decision-related activity in the macaque dorsal visual pathway. Eur. J. Neurosci. 11, 2044–2058 (1999).
Cavanaugh, 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. 88, 2530–2546 (2002).
Celebrini, S. & Newsome, W.T. Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey. J. Neurosci. 14, 4109–4124 (1994).
Britten, K.H., Newsome, W.T., Shadlen, M.N., Celebrini, S. & Movshon, J.A. A relationship between behavioral choice and the visual responses of neurons in macaque MT. Vis. Neurosci. 13, 87–100 (1996).
Shapley, R., Hawken, M. & Ringach, D.L. Dynamics of orientation selectivity in the primary visual cortex and the importance of cortical inhibition. Neuron 38, 689–699 (2003).
Angelucci, A. et al. Circuits for local and global signal integration in primary visual cortex. J. Neurosci. 22, 8633–8646 (2002).
Ferster, D., Chung, S. & Wheat, H. Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380, 249–252 (1996).
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).
Carrasco, M., Ling, S. & Read, S. Attention alters appearance. Nat. Neurosci. 7, 308–313 (2004).
Williford, T. & Maunsell, J.H. Effects of spatial attention on contrast response functions in macaque area V4. J. Neurophysiol. 96, 40–54 (2006).
Buracas, G.T. & Boynton, G.M. The effect of spatial attention on contrast response functions in human visual cortex. J. Neurosci. 27, 93–97 (2007).
Ito, M. & Gilbert, C.D. Attention modulates contextual influences in the primary visual cortex of alert monkeys. Neuron 22, 593–604 (1999).
Xing, J. & Heeger, D.J. Center-surround interactions in foveal and peripheral vision. Vision Res. 40, 3065–3072 (2000).
Freeman, E., Sagi, D. & Driver, J. Lateral interactions between targets and flankers in low-level vision depend on attention to the flankers. Nat. Neurosci. 4, 1032–1036 (2001).
Li, W., Piech, V. & Gilbert, C.D. Perceptual learning and top-down influences in primary visual cortex. Nat. Neurosci. 7, 651–657 (2004).
Everitt, B.J. & Robbins, T.W. Central cholinergic systems and cognition. Annu. Rev. Psychol. 48, 649–684 (1997).
Roberts, M.J. et al. Acetylcholine dynamically controls spatial integration in marmoset primary visual cortex. J. Neurophysiol. 93, 2062–2072 (2005).
Roelfsema, P.R. & van Ooyen, A. Attention-gated reinforcement learning of internal representations for classification. Neural Comput. 17, 2176–2214 (2005).
Thiele, A., Delicato, L.S., Roberts, M.J. & Gieselmann, M.A. A novel electrode-pipette design for simultaneous recording of extracellular spikes and iontophoretic drug application in awake behaving monkeys. J. Neurosci. Methods 158, 207–211 (2006).
Thiele, A., Distler, C., Korbmacher, H. & Hoffmann, K-P. Contribution of inhibitory mechanisms to direction selectivity and response normalization in macaque middle temporal area. Proc. Natl. Acad. Sci. USA 101, 9810–9815 (2004).
Ringach, D. & Shapley, R. Reverse correlation in neurophysiology. Cognit. Sci. 28, 147–166 (2004).
Sceniak, M.P., Hawken, M.J. & Shapley, R. Visual spatial characterization of macaque V1 neurons. J. Neurophysiol. 85, 1873–1887 (2001).
We thank P. Dayan for discussions and comments on the paper. The staff of the Comparative Biology Centre (University of Newcastle upon Tyne) provided excellent technical support. The work was supported by the BBSRC (BBS/B/09325), the Wellcome Trust (070380/Z/03/Z), and the MRC (G0100407; G78/7853).
About this article
Cite this article
Roberts, M., Delicato, L., Herrero, J. et al. Attention alters spatial integration in macaque V1 in an eccentricity-dependent manner. Nat Neurosci 10, 1483–1491 (2007). https://doi.org/10.1038/nn1967
Directed information exchange between cortical layers in macaque V1 and V4 and its modulation by selective attention
Proceedings of the National Academy of Sciences (2021)
Alzheimer's & Dementia (2021)
Contribution of Ionotropic Glutamatergic Receptors to Excitability and Attentional Signals in Macaque Frontal Eye Field
Cerebral Cortex (2021)
Ophthalmic and Physiological Optics (2020)
Scientific Reports (2019)