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Different computations underlie overt presaccadic and covert spatial attention

Abstract

Perception and action are tightly coupled: visual responses at the saccade target are enhanced right before saccade onset. This phenomenon, presaccadic attention, is a form of overt attention—deployment of visual attention with concurrent eye movements. Presaccadic attention is well-documented, but its underlying computational process remains unknown. This is in stark contrast to covert attention—deployment of visual attention without concurrent eye movements—for which the computational processes are well characterized by a normalization model. Here, a series of psychophysical experiments reveal that presaccadic attention modulates visual performance only via response gain changes. A response gain change was observed even when attention field size increased, violating the predictions of a normalization model of attention. Our empirical results and model comparisons reveal that the perceptual modulations by overt presaccadic and covert spatial attention are mediated through different computations.

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Fig. 1: Different forms of attentional modulation on contrast response functions.
Fig. 2: Experiment 1.
Fig. 3: Experiment 2.
Fig. 4: Experiment 2.
Fig. 5: Experiment 3.
Fig. 6: Performance binned by target location in high-uncertainty condition.
Fig. 7: Models and models’ fits.
Fig. 8: Model comparison using AIC.

Data availability

The data that support the findings of this paper are available at https://github.com/hsinhungli/overt-covert-attention.

Code availability

The analysis code used in this paper is available at https://github.com/hsinhungli/overt-covert-attention.

References

  1. 1.

    Kowler, E., Anderson, E., Dosher, B. & Blaser, E. The role of attention in the programming of saccades. Vis. Res. 35, 1897–1916 (1995).

    CAS  PubMed  Article  Google Scholar 

  2. 2.

    Deubel, H. & Schneider, W. X. Saccade target selection and object recognition: evidence for a common attentional mechanism. Vis. Res. 36, 1827–1837 (1996).

    CAS  PubMed  Article  Google Scholar 

  3. 3.

    Hoffman, J. E. & Subramaniam, B. The role of visual attention in saccadic eye movements. Percept. Psychophys. 57, 787–795 (1995).

    CAS  PubMed  Article  Google Scholar 

  4. 4.

    Montagnini, A. & Castet, E. Spatiotemporal dynamics of visual attention during saccade preparation: independence and coupling between attention and movement planning. J. Vis. 7, 8–16 (2007).

    PubMed  Article  Google Scholar 

  5. 5.

    Deubel, H. The time course of presaccadic attention shifts. Psychological Res. 72, 630–640 (2008).

    Article  Google Scholar 

  6. 6.

    Rolfs, M. & Carrasco, M. Rapid simultaneous enhancement of visual sensitivity and perceived contrast during saccade preparation. J. Neurosci. 32, 13744–13752a (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  7. 7.

    Hanning, N. M., Szinte, M. & Deubel, H. Visual attention is not limited to the oculomotor range. Proc. Natl Acad. Sci. USA 116, 9665–9670 (2019).

    CAS  PubMed  Article  Google Scholar 

  8. 8.

    Collins, T., Heed, T., Doré-Mazars, K. & Röder, B. Presaccadic attention interferes with feature detection. Exp. Brain Res. 201, 111–117 (2010).

    PubMed  Article  Google Scholar 

  9. 9.

    Li, H.-H., Barbot, A. & Carrasco, M. Saccade preparation reshapes sensory tuning. Curr. Biol. 26, 1564–1570 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. 10.

    Li, H.-H., Pan, J. & Carrasco, M. Presaccadic attention improves or impairs performance by enhancing sensitivity to higher spatial frequencies. Sci. Rep. 9, 2659 (2019).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  11. 11.

    Ohl, S., Kuper, C. & Rolfs, M. Selective enhancement of orientation tuning before saccades. J. Vis. 17, 2 (2017).

  12. 12.

    Moore, T., Tolias, A. S. & Schiller, P. H. Visual representations during saccadic eye movements. Proc. Natl Acad. Sci. USA 95, 8981–8984 (1998).

    CAS  PubMed  Article  Google Scholar 

  13. 13.

    Mazer, J. A. & Gallant, J. L. Goal-related activity in V4 during free viewing visual search: evidence for a ventral stream visual salience map. Neuron 40, 1241–1250 (2003).

    CAS  PubMed  Article  Google Scholar 

  14. 14.

    Fischer, B. & Boch, R. Enhanced activation of neurons in prelunate cortex before visually guided saccades of trained rhesus monkeys. Exp. Brain Res. 44, 129–137 (1981).

    CAS  PubMed  Article  Google Scholar 

  15. 15.

    Moore, T. & Zirnsak, M. Neural mechanisms of selective visual attention. Annu. Rev. Psychol. 68, 47–72 (2017).

    CAS  PubMed  Article  Google Scholar 

  16. 16.

    Steinmetz, N. A. & Moore, T. Eye movement preparation modulates neuronal responses in area V4 when dissociated from attentional demands. Neuron 83, 496–506 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  17. 17.

    Carrasco, M. Visual attention: the past 25 years. Vis. Res. 51, 1484–1525 (2011).

    PubMed  Article  Google Scholar 

  18. 18.

    Carrasco, M. & Barbot, A. How attention affects spatial resolution. Cold Spring Harb. Symp. Quant. Biol. 79, 149–160 (2015).

  19. 19.

    Maunsell, J. H. Neuronal mechanisms of visual attention. Annu. Rev. Vis. Sci. 1, 373–391 (2015).

    PubMed  Article  Google Scholar 

  20. 20.

    Anton-Erxleben, K. & Carrasco, M. Attentional enhancement of spatial resolution: linking behavioural and neurophysiological evidence. Nat. Rev. Neurosci. 14, 188 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  21. 21.

    Reynolds, J. H. & Heeger, D. J. The normalization model of attention. Neuron 61, 168–185 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  22. 22.

    Lee, J. & Maunsell, J. H. A normalization model of attentional modulation of single unit responses. PLoS ONE 4, e4651 (2009).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  23. 23.

    Verhoef, B.-E. & Maunsell, J. H. Attention-related changes in correlated neuronal activity arise from normalization mechanisms. Nat. Neurosci. 20, 969 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  24. 24.

    Boynton, G. M. A framework for describing the effects of attention on visual responses. Vis. Res. 49, 1129–1143 (2009).

    PubMed  Article  Google Scholar 

  25. 25.

    Kanashiro, T., Ocker, G. K., Cohen, M. R. & Doiron, B. Attentional modulation of neuronal variability in circuit models of cortex. eLife 6, e23978 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  26. 26.

    Williford, T. & Maunsell, J. H. Effects of spatial attention on contrast response functions in macaque area V4. J. Neurophysiol. 96, 40–54 (2006).

    PubMed  Article  Google Scholar 

  27. 27.

    Martınez-Trujillo, J. C. & Treue, S. Attentional modulation strength in cortical area MT depends on stimulus contrast. Neuron 35, 365–370 (2002).

    PubMed  Article  Google Scholar 

  28. 28.

    McAdams, C. J. & Maunsell, J. H. Effects of attention on orientation-tuning functions of single neurons in macaque cortical area V4. J. Neurosci. 19, 431–441 (1999).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  29. 29.

    Sani, I., Santandrea, E., Morrone, M. C. & Chelazzi, L. Temporally evolving gain mechanisms of attention in macaque area V4. J. Neurophysiol. 118, 964–985 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  30. 30.

    Reynolds, J. H., Pasternak, T. & Desimone, R. Attention increases sensitivity of V4 neurons. Neuron 26, 703–714 (2000).

    CAS  PubMed  Article  Google Scholar 

  31. 31.

    Ling, S. & Carrasco, M. Sustained and transient covert attention enhance the signal via different contrast response functions. Vis. Res. 46, 1210–1220 (2006).

    PubMed  Article  Google Scholar 

  32. 32.

    Dosher, B. A. & Lu, Z.-L. Noise exclusion in spatial attention. Psychological Sci. 11, 139–146 (2000).

    CAS  Article  Google Scholar 

  33. 33.

    Lu, Z.-L. & Dosher, B. A. External noise distinguishes attention mechanisms. Vis. Res. 38, 1183–1198 (1998).

    CAS  PubMed  Article  Google Scholar 

  34. 34.

    Huang, L. & Dobkins, K. R. Attentional effects on contrast discrimination in humans: evidence for both contrast gain and response gain. Vis. Res. 45, 1201–1212 (2005).

    PubMed  Article  Google Scholar 

  35. 35.

    Morrone, M. C., Denti, V. & Spinelli, D. Different attentional resources modulate the gain mechanisms for color and luminance contrast. Vis. Res. 44, 1389–1401 (2004).

    CAS  PubMed  Article  Google Scholar 

  36. 36.

    Cameron, E. L., Tai, J. C. & Carrasco, M. Covert attention affects the psychometric function of contrast sensitivity. Vis. Res. 42, 949–967 (2002).

    PubMed  Article  Google Scholar 

  37. 37.

    Pestilli, F., Ling, S. & Carrasco, M. A population-coding model of attention’s influence on contrast response: estimating neural effects from psychophysical data. Vis. Res. 49, 1144–1153 (2009).

    PubMed  Article  Google Scholar 

  38. 38.

    Pestilli, F., Viera, G. & Carrasco, M. How do attention and adaptation affect contrast sensitivity? J. Vis. 7, 9–12 (2007).

    PubMed  PubMed Central  Article  Google Scholar 

  39. 39.

    Herrmann, K., Heeger, D. J. & Carrasco, M. Feature-based attention enhances performance by increasing response gain. Vis. Res. 74, 10–20 (2012).

    PubMed  Article  Google Scholar 

  40. 40.

    Herrmann, K., Montaser-Kouhsari, L., Carrasco, M. & Heeger, D. J. When size matters: attention affects performance by contrast or response gain. Nat. Neurosci. 13, 1554–1559 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  41. 41.

    Fernández, A. & Carrasco, M. Extinguishing exogenous attention via transcranial magnetic stimulation. Curr. Biol. 30, 4078–4084. e4073 (2020).

    PubMed  Article  CAS  Google Scholar 

  42. 42.

    Jigo, M. & Carrasco, M. Differential impact of exogenous and endogenous attention on the contrast sensitivity function across eccentricity. J. Vis. 20, 11 (2020).

  43. 43.

    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).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  44. 44.

    Murray, S. O. The effects of spatial attention in early human visual cortex are stimulus independent. J. Vis. 8, 2–11 (2008).

    PubMed  Article  Google Scholar 

  45. 45.

    Li, X., Lu, Z.-L., Tjan, B. S., Dosher, B. A. & Chu, W. Blood oxygenation level-dependent contrast response functions identify mechanisms of covert attention in early visual areas. Proc. Natl Acad. Sci. USA 105, 6202–6207 (2008).

    CAS  PubMed  Article  Google Scholar 

  46. 46.

    Pestilli, F., Carrasco, M., Heeger, D. J. & Gardner, J. L. Attentional enhancement via selection and pooling of early sensory responses in human visual cortex. Neuron 72, 832–846 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  47. 47.

    Lu, Z.-L., Li, X., Tjan, B. S., Dosher, B. A. & Chu, W. Attention extracts signal in external noise: a BOLD fMRI study. J. Cogn. Neurosci. 23, 1148–1159 (2011).

    PubMed  Article  Google Scholar 

  48. 48.

    Schwedhelm, P., Krishna, B. S. & Treue, S. An extended normalization model of attention accounts for feature-based attentional enhancement of both response and coherence gain. PLoS Comput. Biol. 12, e1005225 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  49. 49.

    Ni, A. M. & Maunsell, J. H. Spatially tuned normalization explains attention modulation variance within neurons. J. Neurophysiol. 118, 1903–1913 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  50. 50.

    Verhoef, B.-E. & Maunsell, J. H. Attention operates uniformly throughout the classical receptive field and the surround. eLife 5, e17256 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  51. 51.

    Ni, A. M. & Maunsell, J. H. Neuronal effects of spatial and feature attention differ due to normalization. J. Neurosci. 39, 5493–5505 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  52. 52.

    Ni, A. M., Ray, S. & Maunsell, J. H. Tuned normalization explains the size of attention modulations. Neuron 73, 803–813 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  53. 53.

    Szinte, M., Carrasco, M., Cavanagh, P. & Rolfs, M. Attentional trade-offs maintain the tracking of moving objects across saccades. J. Neurophysiol. 113, 2220–2231 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  54. 54.

    Cutrone, E. K., Heeger, D. J. & Carrasco, M. On spatial attention and its field size on the repulsion effect. J. Vis. 18, 8 (2018).

  55. 55.

    Carandini, M. & Heeger, D. J. Normalization as a canonical neural computation. Nat. Rev. Neurosci. 13, 51–62 (2012).

    CAS  Article  Google Scholar 

  56. 56.

    Cutrone, E. K., Heeger, D. J. & Carrasco, M. Attention enhances contrast appearance via increased input baseline of neural responses. J. Vis. 14, 16 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  57. 57.

    Hara, Y., Pestilli, F. & Gardner, J. L. Differing effects of attention in single-units and populations are well predicted by heterogeneous tuning and the normalization model of attention. Front. Computational Neurosci. 8, 12 (2014).

    Article  Google Scholar 

  58. 58.

    Akaike, H. in Selected Papers of Hirotugu Akaike (eds Parzen, E. et al.) 199–213 (Springer, 1998).

  59. 59.

    Akaike, H. in Selected Papers of Hirotugu Akaike (eds Parzen, E. et al.) 215–222 (Springer, 1974).

  60. 60.

    Poletti, M., Rucci, M. & Carrasco, M. Selective attention within the foveola. Nat. Neurosci. 20, 1413–1417 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  61. 61.

    Klapetek, A., Jonikaitis, D. & Deubel, H. Attention allocation before antisaccades. J. Vis. 16, 11 (2016).

    PubMed  Article  Google Scholar 

  62. 62.

    Van der Stigchel, S. & De Vries, J. There is no attentional global effect: attentional shifts are independent of the saccade endpoint. J. Vis. 15, 17 (2015).

  63. 63.

    Wollenberg, L., Deubel, H. & Szinte, M. Visual attention is not deployed at the endpoint of averaging saccades. PLoS Biol. 16, e2006548 (2018).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  64. 64.

    Van der Stigchel, S. & de Vries, J. Commentary: visual attention is not deployed at the endpoint of averaging saccades. Front. Psychol. 9, 2166 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  65. 65.

    Findlay, J. M. Global visual processing for saccadic eye movements. Vis. Res. 22, 1033–1045 (1982).

    CAS  PubMed  Article  Google Scholar 

  66. 66.

    Coren, S. & Hoenig, P. Effect of non-target stimuli upon length of voluntary saccades. Percept. Mot. Skills 34, 499–508 (1972).

    CAS  PubMed  Article  Google Scholar 

  67. 67.

    Steinmetz, N. A. & Moore, T. Changes in the response rate and response variability of area V4 neurons during the preparation of saccadic eye movements. J. Neurophysiol. 103, 1171–1178 (2010).

    PubMed  Article  Google Scholar 

  68. 68.

    Lisi, M., Solomon, J. A. & Morgan, M. J. Gain control of saccadic eye movements is probabilistic. Proc. Natl Acad. Sci. USA 116, 16137–16142 (2019).

    CAS  PubMed  Article  Google Scholar 

  69. 69.

    Hanning, N. M., Aagten-Murphy, D. & Deubel, H. Independent selection of eye and hand targets suggests effector-specific attentional mechanisms. Sci. Rep. 8, 9434 (2018).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  70. 70.

    Castet, E., Jeanjean, S., Montagnini, A., Laugier, D. & Masson, G. S. Dynamics of attentional deployment during saccadic programming. J. Vis. 6, 196–212 (2006).

  71. 71.

    Shimozaki, S. S., Schoonveld, W. A. & Eckstein, M. P. A unified Bayesian observer analysis for set size and cueing effects on perceptual decisions and saccades. J. Vis. 12, 27–27 (2012).

    PubMed  Article  Google Scholar 

  72. 72.

    Kustov, A. A. & Robinson, D. L. Shared neural control of attentional shifts and eye movements. Nature 384, 74–77 (1996).

    CAS  PubMed  Article  Google Scholar 

  73. 73.

    Ikkai, A. & Curtis, C. E. Common neural mechanisms supporting spatial working memory, attention and motor intention. Neuropsychologia 49, 1428–1434 (2011).

    PubMed  Article  Google Scholar 

  74. 74.

    Armstrong, K. M., Fitzgerald, J. K. & Moore, T. Changes in visual receptive fields with microstimulation of frontal cortex. Neuron 50, 791–798 (2006).

    CAS  PubMed  Article  Google Scholar 

  75. 75.

    Armstrong, K. M. & Moore, T. Rapid enhancement of visual cortical response discriminability by microstimulation of the frontal eye field. Proc. Natl Acad. Sci. USA 104, 9499–9504 (2007).

    CAS  PubMed  Article  Google Scholar 

  76. 76.

    Engel, T. A. et al. Selective modulation of cortical state during spatial attention. Science 354, 1140–1144 (2016).

    CAS  PubMed  Article  Google Scholar 

  77. 77.

    Zhao, M., Gersch, T. M., Schnitzer, B. S., Dosher, B. A. & Kowler, E. Eye movements and attention: the role of pre-saccadic shifts of attention in perception, memory and the control of saccades. Vis. Res. 74, 40–60 (2012).

    PubMed  Article  Google Scholar 

  78. 78.

    Gregoriou, G. G., Gotts, S. J. & Desimone, R. Cell-type-specific synchronization of neural activity in FEF with V4 during attention. Neuron 73, 581–594 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  79. 79.

    Thompson, K. G., Biscoe, K. L. & Sato, T. R. Neuronal basis of covert spatial attention in the frontal eye field. J. Neurosci. 25, 9479–9487 (2005).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  80. 80.

    Juan, C.-H., Shorter-Jacobi, S. M. & Schall, J. D. Dissociation of spatial attention and saccade preparation. Proc. Natl Acad. Sci. USA 101, 15541–15544 (2004).

    CAS  PubMed  Article  Google Scholar 

  81. 81.

    Lowe, K. A. & Schall, J. D. Functional categories of visuomotor neurons in macaque frontal eye field. eNeuro 5, https://doi.org/10.1523/ENEURO.0131-18.2018 (2018).

  82. 82.

    Moore, T. Shape representations and visual guidance of saccadic eye movements. Science 285, 1914–1917 (1999).

    CAS  PubMed  Article  Google Scholar 

  83. 83.

    Saber, G. T., Pestilli, F. & Curtis, C. E. Saccade planning evokes topographically specific activity in the dorsal and ventral streams. J. Neurosci. 35, 245–252 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  84. 84.

    Moore, T. & Chang, M. H. Presaccadic discrimination of receptive field stimuli by area V4 neurons. Vis. Res. 49, 1227–1232 (2009).

    PubMed  Article  Google Scholar 

  85. 85.

    Kleiner, M. et al. What’s new in Psychtoolbox-3. Perception 36, 1–16 (2007).

    Google Scholar 

  86. 86.

    Watson, A. B. & Pelli, D. G. QUEST: a Bayesian adaptive psychometric method. Percept. Psychophys. 33, 113–120 (1983).

    CAS  PubMed  Article  Google Scholar 

  87. 87.

    JASP v.0.14.1 (JASP-Stats.org, 2020).

  88. 88.

    Engbert, R. & Mergenthaler, K. Microsaccades are triggered by low retinal image slip. Proc. Natl Acad. Sci. USA 103, 7192–7197 (2006).

    CAS  PubMed  Article  Google Scholar 

  89. 89.

    Graf, A. B., Kohn, A., Jazayeri, M. & Movshon, J. A. Decoding the activity of neuronal populations in macaque primary visual cortex. Nat. Neurosci. 14, 239–245 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  90. 90.

    Keliris, G. A., Li, Q., Papanikolaou, A., Logothetis, N. K. & Smirnakis, S. M. Estimating average single-neuron visual receptive field sizes by fMRI. Proc. Natl Acad. Sci. USA 116, 6425–6434 (2019).

    CAS  PubMed  Article  Google Scholar 

  91. 91.

    Jazayeri, M. & Movshon, J. A. Optimal representation of sensory information by neural populations. Nat. Neurosci. 9, 690–696 (2006).

    CAS  PubMed  Article  Google Scholar 

  92. 92.

    Acerbi, L. & Ma, W. J. Practical Bayesian optimization for model fitting with Bayesian adaptive direct search. In Proc. Advances in Neural Information Processing Systems (eds Guyon, I. et al.) 1836–1846 (NIPS, 2017).

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Acknowledgements

This work was supported by National Institutes of Health grant R01EY019693 (to M.C.). H.-H.L. was supported by NIH grant R90DA043849. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the paper. We thank members of the Carrasco Laboratory, in particular A. Fernández, N. Hanning and M. Jigo.

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H.-H.L. and M.C. conceptualized and designed the experiments. H.-H.L. and J.P. conducted the experiments and analysed the data. H.-H.L., J.P. and M.C. wrote the paper.

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Correspondence to Hsin-Hung Li.

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Peer review information Nature Human Behaviour thanks Tirin Moore and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Li, HH., Pan, J. & Carrasco, M. Different computations underlie overt presaccadic and covert spatial attention. Nat Hum Behav (2021). https://doi.org/10.1038/s41562-021-01099-4

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