Attention modulates spatial priority maps in the human occipital, parietal and frontal cortices
Thomas C Sprague, John T Serences, Thomas C Sprague, John T Serences
Abstract
Computational theories propose that attention modulates the topographical landscape of spatial 'priority' maps in regions of the visual cortex so that the location of an important object is associated with higher activation levels. Although studies of single-unit recordings have demonstrated attention-related increases in the gain of neural responses and changes in the size of spatial receptive fields, the net effect of these modulations on the topography of region-level priority maps has not been investigated. Here we used functional magnetic resonance imaging and a multivariate encoding model to reconstruct spatial representations of attended and ignored stimuli using activation patterns across entire visual areas. These reconstructed spatial representations reveal the influence of attention on the amplitude and size of stimulus representations within putative priority maps across the visual hierarchy. Our results suggest that attention increases the amplitude of stimulus representations in these spatial maps, particularly in higher visual areas, but does not substantively change their size.
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References
- Koch C, Ullman S. Shifts in selective visual attention: towards the underlying neural circuitry. Hum Neurobiol. 1985;4:219–227.
- Itti L, Koch C, Niebur E. A model of saliency-based visual attention for rapid scene analysis. Pattern Analysis and Machine Intelligence, IEEE Transactions on. 1998;20:1254–1259.
- Itti L, Koch C. Computational modelling of visual attention. Nat Rev Neurosci. 2001;2:194–203.
- Serences JT, Yantis S. Selective visual attention and perceptual coherence. Trends in cognitive sciences. 2006;10:38–45.
- Fecteau JH, Munoz DP. Salience, relevance, and firing: a priority map for target selection. Trends in Cognitive Sciences. 2006;10:382–390.
- Bichot NP, Schall JD. Effects of similarity and history on neural mechanisms of visual selection. Nat Neurosci. 1999;2:549–554.
- Luck SJ, Chelazzi L, Hillyard SA, Desimone R. Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. Journal of Neurophysiology. 1997;77:24–42.
- Reynolds JH, Chelazzi L, Desimone R. Competitive mechanisms subserve attention in macaque areas V2 and V4. The Journal of Neuroscience. 1999;19:1736–1753.
- McAdams CJ, Maunsell JHR. Effects of Attention on Orientation-Tuning Functions of Single Neurons in Macaque Cortical Area V4. The Journal of Neuroscience. 1999;19:431–441.
- Connor CE, Preddie DC, Gallant JL, Van Essen DC. Spatial attention effects in macaque area V4. The Journal of Neuroscience. 1997;17:3201–3214.
- Treue S, Maunsell JHR. Attentional modulation of visual motion processing in cortical areas MT and MST. Nature. 1996;382:539–541.
- Reynolds JH, Pasternak T, Desimone R. Attention increases sensitivity of V4 neurons. Neuron. 2000;26:703–714.
- McAdams CJ, Maunsell JHR. Attention to both space and feature modulates neuronal responses in macaque area V4. Journal of Neurophysiology. 2000;83:1751–1755.
- Treue S, Maunsell JHR. Effects of attention on the processing of motion in macaque middle temporal and medial superior temporal visual cortical areas. The Journal of Neuroscience. 1999;19:7591–7602.
- Seidemann E, Newsome WT. Effect of spatial attention on the responses of area MT neurons. Journal of Neurophysiology. 1999;81:1783–1794.
- Motter BC. Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. Journal of neurophysiology. 1993;70:909–19.
- Moran J, Desimone R. Selective attention gates visual processing in the extrastriate cortex. Science. 1985;229:782–784.
- Saproo S, Serences JT. Spatial Attention Improves the Quality of Population Codes in Human Visual Cortex. Journal of Neurophysiology. 2010;104:885–895.
- Womelsdorf T, Anton-Erxleben K, Pieper F, Treue S. Dynamic shifts of visual receptive fields in cortical area MT by spatial attention. Nature Neuroscience. 2006;9:1156–1160.
- Womelsdorf T, Anton-Erxleben K, Treue S. Receptive Field Shift and Shrinkage in Macaque Middle Temporal Area through Attentional Gain Modulation. The Journal of Neuroscience. 2008;28:8934–8944.
- Anton-Erxleben K, Stephan VM, Treue S. Attention reshapes center-surround receptive field structure in macaque cortical area MT. Cerebral Cortex. 2009;19:2466–2478.
- Niebergall R, Khayat PS, Treue S, Martinez-Trujillo JC. Expansion of MT Neurons Excitatory Receptive Fields during Covert Attentive Tracking. The Journal of Neuroscience. 2011;31:15499–15510.
- Anton-Erxleben K, Carrasco M. Attentional enhancement of spatial resolution: linking behavioural and neurophysiological evidence. Nature Reviews Neuroscience. 2013;14:188–200.
- Liu T, Pestilli F, Carrasco M. Transient attention enhances perceptual performance and FMRI response in human visual cortex. Neuron. 2005;45:469–477.
- Gandhi SP, Heeger DJ, Boynton GM. Spatial attention affects brain activity in human primary visual cortex. Proceedings of the National Academy of Sciences of the United States of America. 1999;96:3314–3319.
- Kastner S, Pinsk MA, De Weerd P, Desimone R, Ungerleider LG. Increased activity in human visual cortex during directed attention in the absence of visual stimulation. Neuron. 1999;22:751–761.
- Brefczynski JA, DeYoe EA. A physiological correlate of the “spotlight” of visual attention. Nature Neuroscience. 1999;2:370–374.
- Silver MA, Ress D, Heeger DJ. Neural correlates of sustained spatial attention in human early visual cortex. Journal of Neurophysiology. 2007;97:229–237.
- Tootell RB, et al. The retinotopy of visual spatial attention. Neuron. 1998;21:1409–1422.
- Murray SO. The effects of spatial attention in early human visual cortex are stimulus independent. Journal of Vision. 2008;8:2.1–11.
- Silver MA, Ress D, Heeger DJ. Topographic maps of visual spatial attention in human parietal cortex. Journal of Neurophysiology. 2005;94:1358–1371.
- Jerde TA, Merriam EP, Riggall AC, Hedges JH, Curtis CE. Prioritized Maps of Space in Human Frontoparietal Cortex. The Journal of Neuroscience. 2012;32:17382–17390.
- Jehee JFM, Brady DK, Tong F. Attention Improves Encoding of Task-Relevant Features in the Human Visual Cortex. The Journal of Neuroscience. 2011;31:8210–8219.
- Serences JT, Saproo S. Computational advances towards linking BOLD and behavior. Neuropsychologia. 2011;50:435–446.
- Awh E, Jonides J. Overlapping mechanisms of attention and spatial working memory. Trends in Cognitive Sciences. 2001;5:119–126.
- Brouwer G, Heeger D. Decoding and Reconstructing Color from Responses in Human Visual Cortex. Journal of Neuroscience. 2009;29:13992–14003.
- Naselaris T, Kay K, Nishimoto S, Gallant J. Encoding and decoding in fMRI. Neuroimage. 2011;56:400–410.
- Scolari M, Byers A, Serences JT. Optimal Deployment of Attentional Gain during Fine Discriminations. Journal of Neuroscience. 2012;32:1–11.
- Gattass R, et al. Cortical visual areas in monkeys: location, topography, connections, columns, plasticity and cortical dynamics. Philosophical Transactions of the Royal Society B: Biological Sciences. 2005;360:709–731.
- Ben Hamed S, Duhamel JR, Bremmer F, Graf W. Visual receptive field modulation in the lateral intraparietal area during attentive fixation and free gaze. Cerebral cortex. 2002;12:234–245.
- Mohler CW, Goldberg ME, Wurtz RH. Visual receptive fields of frontal eye field neurons. Brain Research. 1973;61:385–389.
- Dumoulin S, Wandell B. Population receptive field estimates in human visual cortex. NeuroImage. 2008;39:647–660.
- Sereno MI, Pitzalis S, Martinez A. Mapping of Contralateral Space in Retinotopic Coordinates by a Parietal Cortical Area in Humans. Science. 2001;294:1350–1354.
- Swisher JD, Halko MA, Merabet LB, McMains SA, Somers DC. Visual topography of human intraparietal sulcus. The Journal of Neuroscience. 2007;27:5326–5337.
- Saygin AP, Sereno MI. Retinotopy and Attention in Human Occipital, Temporal, Parietal, and Frontal Cortex. Cerebral Cortex. 2008;18:2158–2168.
- Kastner S, et al. Modulation of sensory suppression: implications for receptive field sizes in the human visual cortex. Journal of Neurophysiology. 2001;86:1398–1411.
- Srimal R, Curtis CE. Persistent neural activity during the maintenance of spatial position in working memory. NeuroImage. 2008;39:455–468.
- Paus T. Location and function of the human frontal eye-field: A selective review. Neuropsychologia. 1996;34:475–483.
- Kastner S, et al. Topographic Maps in Human Frontal Cortex Revealed in Memory-Guided Saccade and Spatial Working-Memory Tasks. Journal of Neurophysiology. 2007;97:3494–3507.
- Fischer J, Whitney D. Attention Narrows Position Tuning of Population Responses in V1. Current biology. 2009;19:1356–1361.
- Engel SA, et al. fMRI of human visual cortex. Nature. 1994;369:525.
- Sereno MI, et al. Borders of Multiple Visual Areas in Humans Revealed by Functional Magnetic Resonance Imaging. Science. 1995;268:889–893.
- Tootell RB, et al. Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. The Journal of Neuroscience. 1995;15:3215–3230.
- Serences JT, Boynton GM. The representation of behavioral choice for motion in human visual cortex. The Journal of Neuroscience. 2007;27:12893–12899.
- Kay K, Naselaris T, Prenger R, Gallant J. Identifying natural images from human brain activity. Nature. 2008;452:352–355.
- Hoerl AE, Kennard RW. Ridge Regression: Biased Estimation for Nonorthogonal Problems. Technometrics. 1970;12:55–67.
- Lee S, Papanikolaou A, Logothetis NK, Smirnakis SM, Keliris Ga. A new method for estimating population receptive field topography in visual cortex. NeuroImage. 2013;81:144–157.
- Schwarz G. Estimating the Dimension of a Model. The Annals of Statistics. 1978;6:461–464.
- Benjamini Y, Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Annals of statistics. 2001;29:1165–1188.
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