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Differential Impact of Endogenous and Exogenous Attention on Activity In bioRxiv preprint doi: https://doi.org/10.1101/414508; this version posted November 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Differential impact of endogenous and exogenous attention 2 on activity in human visual cortex 3 4 Laura Dugué1,2,3,4, Elisha P. Merriam1,2,5, David J. Heeger1,2 & Marisa Carrasco1,2 5 6 7 8 9 10 1 Department of Psychology, New York University 11 2 Center for Neural Science, New York University 12 3 Université de Paris, CNRS, Integrative Neuroscience and Cognition Center, F-75006 Paris, 13 France 14 4 Institut Universitaire de France, Paris, France 15 5 Laboratory of Brain and Cognition, NIMH/NIH, Bethesda, MD 16 17 18 Running title: endogenous and exogenous attention 19 20 21 Corresponding author: 22 Laura Dugué 23 Current address: 45 rue des Saints-Pères 75006 Paris, FRANCE 24 [email protected] 1 bioRxiv preprint doi: https://doi.org/10.1101/414508; this version posted November 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 25 ABSTRACT (150 words) 26 How do endogenous (voluntary) and exogenous (involuntary) attention modulate activity in vis- 27 ual cortex? Using ROI-based fMRI analysis, we measured fMRI activity for valid and invalid 28 trials (target at cued/un-cued location, respectively), pre- or post-cueing endogenous or exoge- 29 nous attention, while participants performed the same orientation discrimination task. We found 30 stronger modulation in contralateral than ipsilateral visual regions, and higher activity in valid- 31 than invalid-trials. For endogenous attention, modulation of stimulus-evoked activity due to a 32 pre-cue increased along the visual hierarchy, but was constant due to a post-cue. For exoge- 33 nous attention, modulation of stimulus-evoked activity due to a pre-cue was constant along the 34 visual hierarchy, but was not modulated due to a post-cue. These findings reveal that endoge- 35 nous and exogenous attention distinctly modulate activity in visuo-occipital areas during orient- 36 ing and reorienting; endogenous attention facilitates both the encoding and the readout of visu- 37 al information whereas exogenous attention only facilitates the encoding of information. 38 39 Keywords: exogenous attention, endogenous attention, fMRI activity, occipital visual areas, 40 top-down processing, bottom-up processing. 2 bioRxiv preprint doi: https://doi.org/10.1101/414508; this version posted November 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 41 INTRODUCTION 42 Spatial, covert visual attention is the selective processing of visual information in space, 43 without change in gaze. Attention can be allocated voluntarily –endogenous attention– or invol- 44 untarily –exogenous attention. Endogenous and exogenous attention have different temporal 45 dynamics; endogenous takes about 300 ms to be deployed and can be sustained at will where- 46 as exogenous attention takes only about 100 ms to be deployed and it is transient (for reviews 47 see 1,2). These two types of attention often have similar perceptual consequences (reviews by 48 1,2), but notable exceptions indicate that whereas endogenous attention acts in a flexible way, 49 exogenous attention acts in an inflexible or automatic way. For instance: (a) The benefits and 50 costs in perception (discriminability and speed of information accrual) scale with cue validity for 51 endogenous but not for exogenous attention (e.g. 3); (b) The effects of covert attention on con- 52 trast sensitivity often differ for endogenous and exogenous attention (e.g. 4-9); and (c) For a 53 texture segmentation task in which heightened spatial resolution improves or impairs perfor- 54 mance as a function of target eccentricity, endogenous attention improves performance across 55 eccentricity, whereas exogenous attention improves performance at peripheral locations where 56 resolution is poor, it hampers performance where resolution is already high for the task at hand 57 (e.g. 10-15). 58 Basic visual processes, such as contrast sensitivity and spatial resolution, are mediated 59 by activity in early visual cortex, and are altered by covert attention (reviews by 1,2,16,17). Specifi- 60 cally, single-unit studies in monkeys have demonstrated effects of endogenous attention in oc- 61 cipital areas (e.g. 18-25). Additionally, fMRI studies have shown that endogenous attention caus- 62 es a baseline shift in early visual areas (e.g. 26-32; review by 33) and increases the dynamic 63 range of fMRI responses 34,35. Comparatively, little is known about the effect of exogenous at- 64 tention on visual areas both from single-unit studies 36,37 and fMRI studies (for reviews see 1,16). 65 Since Corbetta and Schulman’s seminal review (2002) 38 on the neural bases of endog- 66 enous and exogenous attention, there has been emphasis on characterizing networks of brain 67 regions within the frontal and parietal lobes (for reviews see 33,39,40). Yet, there remains consid- 68 erable debate regarding the dissociation between dorsal regions, for endogenous attention, and 3 bioRxiv preprint doi: https://doi.org/10.1101/414508; this version posted November 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 69 ventral regions, for exogenous attention (e.g. 40,41), including the role of the temporo-parietal 70 junction (TPJ; 42-45). Classically, researchers have described endogenous attention as a top- 71 down process, and exogenous attention as a bottom-up process 1,38-40,46-48. This characteriza- 72 tion originated in psychophysics experiments, and was then studied using fMRI, in which the 73 two types of attention have been often investigated separately (for reviews 1,33,39,46). 74 Studies of endogenous and exogenous attention focusing on parietal and frontal areas 75 have shown that the two types of attention differentially modulate fronto-parietal connectivity 76 40,49. For example, there are critical differences in the temporal order of neural responses in 77 frontal and parietal cortex in monkeys between these attention conditions, i.e. frontal activity 78 precedes parietal activity during endogenous attentional orienting, whereas parietal activity 79 precedes frontal activity during exogenous orienting. Critically, it is often assumed that the ef- 80 fects of endogenous and exogenous attention are the same in striate and extra-striate areas 81 33,38,39,50,51. 82 A number of important considerations limit the conclusions that may be drawn from the 83 few studies that have directly compared independent effects of visual exogenous and endoge- 84 nous spatial attention 40,51-53: 85 (1) The effect of attention on behavioral performance was assessed in some studies with a 86 detection task using RT as their only dependent variable 51,53, in which performance may 87 differ due to speed of processing, discriminability or criterion 54-56 and/or motor behavior 88 57,58. 89 (2) In the studies in which performance was assessed in a discrimination task using RT 52, 90 small RT differences were reported, which could have resulted from speed of pro- 91 cessing, discriminability, or criterion factors 54-56. 92 (3) In the studies in which accuracy was not assessed 40,51,53, it is not possible to know 93 whether task difficulty was the same for both types of attention, and task difficulty can 94 interact with the strength of fMRI activity 59,60. 4 bioRxiv preprint doi: https://doi.org/10.1101/414508; this version posted November 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 95 (4) For the studies in which eye position was not monitored while participants performed the 96 task in the scanner 40,51-53, the results could be due to covert attention, overt attention or 97 both 1,61,62. 98 (5) Given that exogenous attention is a fast, transient process (for reviews see 1,2,16,17), it 99 was inappropriately manipulated in the studies in which long stimulus onset asynchro- 100 nies (SOA) were used 51,52,63-65 making the comparison between the two attention condi- 101 tions problematic. 102 (6) Except for two studies, one interested in attentional modulation in the Fusiform Face Ar- 103 ea (FFA) 65 and the other in the TPJ 42, statistical parametric mapping was applied to 104 group averaged data to identify regions of the brain that were active during task perfor- 105 mance. Some found significant activity in the occipital pole 51-53, but attentional modula- 106 tion of fMRI activity was not systematically assessed across different visual areas. 107 Given all these methodological limitations, it is unknown how these two types of atten- 108 tion affect neural activity in each individual visuo-occipital area, and how modulation of activity 109 in visual cortex is linked to changes in perceptual performance.
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