Attention But Not Awareness Modulates the BOLD Signal in the Human V1 During Binocular Suppression Masataka Watanabe

, et al. Science 334, 829 (2011); DOI: 10.1126/science.1203161

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Wherry. Dienz et al. Zuniga. Crotty. Nat. 17. Wako. 39. M. I. Nat. Crotty (La Jolla Institute of Allergy and Immunology) for providing IL-6R ko. 2Max Planck Institute for Biological Cybernetics. Elsaesser. E. L. Johnston et al. A. Brooks. Immunol.REPORTS in these contexts remain elusive (43–45). Y. R. L. E. Netski et al. 932 (2011). A and B. Tokyo. A. 10. H. Med. B. 98. we presented a motion grating in one eye as the perceptual target.Z. 10514 (2005). 19. while they invite a reconsideration of the functional role of V1 in visual awareness. Top-down attention directed toward percep1 A School of Engineering.Z. Our results agree with previously reported V1 BOLD effects on attention. This work was supported by grants from the NIH (AI072752 and AI081923 to E.S. 174. University of Tokyo. Natl. Immunol. Despite the relatively large monocular region (6° in diameter). F. M. We thus implemented a modified version of continuous flash suppression [see supporting online material (SOM)] that can constantly render a motion target stimulus invisible (22. J. G. However. whereas the gist of scenes can be perceived despite the near absence of attention (4–7). The difference in the lower-level limit of BOLD activation between attention and awareness illustrates dissociated neural correlates of the two processes. Nascimbeni. M. Goonetilleke.I. N. Ahmed. B.1174182. 374 (2008). Poholek et al. R. Drew (University of Cincinnati). 339 (1994). 33. the target as a whole could still be rendered invisible (see below for behavioral results). 14. V. 32. Suto et al. E. PLoS Biol. 1. B. Boosting IL-6 signaling in CD4 T cells and/or the downstream TFH responses could aid therapies to combat persistent viruses. Yu et al. Proc. C. S1 to S23 Table S1 References 16 May 2011. Science 324. M. D. Nat. I. Czar et al. 21. K. Immunol.3 Takeshi Asamizuya. Chehimi et al. 41. 7219 (2010). D. recent progress in psychophysics indicates that visual attention and visual awareness are two dissociated functions in the visual system (1).I. Acad. 41.. 4.. 10. Acknowledgments: The data reported in this paper are tabulated in the supporting online material. Kranich et al. 16. 11 NOVEMBER 2011 829 Downloaded from www. J. 1006 (2009).. U. Y. 9. Until on November 13. G. D. Immunity 34. as in the case of pattern rivalry (24). 16. Manchester. Exp. stat3 ko... 40. M. 682 (2006).3*† Kang Cheng. J. Y. R.1+ Smarta mice. 1 (2005). 3. Nurieva et al.. 44. D. Letvin. Dolgoter for technical assistance throughout. Sci. †To whom correspondence should be addressed. 185. 160. 5526 (2005). J. 21. 184. D.1208421 Attention But Not Awareness Modulates the BOLD Signal in the Human V1 During Binocular Suppression Masataka Watanabe. J. and S. 1572 (2009). Med. 6°. Y. Haynes. 5. Alcalde. A.3* Yusuke Murayama. when we attend to an object. Korn et al. Sci. and being aware of an object may lead to attention directed toward it. Int. 61/475. L. Immunity 31. Wu et al. N. Deenick et al.. 36. E. E. M.H. T. the target remained visible (Fig. 2. 31. 1293 (2008). 1B) (SOM). J. S. M. M. J. Salmi. We used a block-design paradigm. L. Crotty for insightful discussion. 38. 241 (2010). 10. Exp. Aubert. 205. J. Immunol. respectively. A. 492 (2011). Acad. 1576 (2009). J. J. Exp. Japan. 40 (2002). We focused on V1 because measurements from neuroimaging and electrophysiology are incongruent for both attention (8–15) and awareness (16–21). Du. A. Mack. Fahey et al. We separately examined the effects of topdown attention and visual awareness on the blood oxygenation level–dependent (BOLD) signal in the human primary visual cortex (V1). 733 (2011). Blood 108. 26. Cell Host Microbe 4. www. 521 (1984). Infect. D. 18. Saitama. Kishimoto. J. Conry et al. L. Liou. Immunol. W. Med. B. Kopf et al. Oldstone. 987 (2011). Ahmed. 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REPORTS contained 16 presentations of visible stimuli or invisible stimuli as described above (Fig. Attention was manipulated by asking the participant to switch between two behavioral tasks. 1. thus ensuring that the visibility and/or invisibility of the target were indeed as intended. ventral V1.” two invisible stimuli were intermingled with remaining 14 visible stimuli as catch trials in a pseudo-randomized order. Video frames of the two stimuli were similarly interleaved to match the contents of the visible stimulus.7ms 16s percent signal change (%) D 10 E 5 4 3 2 1 0 -1 -2 -5 0 5 10 15 20 25 30 V1d CS L V1v V1d CS L V1v Fig. and blue char- 3 time (s) acters required the participant to perform a letter detection task [as exemplified in (B)]. Additional experiments with simultaneously measured eye positions have ruled out the possibility that the A i visible stimuli B invisible stimuli C visible stimuli (1s) visible stimuli (1s) h m c m m c c 50 0m typical percept i i h h visible stimulus block invisible stimulus block dominant eye non-dominant eye 16.05. Likewise in the “invisible stimulus block. In contrast. C and D. the invisible stimulus in the attention to target condition led to an increased BOLD signal as compared to the visible stimulus (P < 0. Red pixels indicate the targeted monocular region activated by a disk-shaped counter-phasing checkerboard. 2). SCIENCE www.” two visible stimuli were mixed with remaining 14 invisible stimuli. and that the person’s attention was faithfully directed toward the central fixation in attention to nontarget blocks. we compared measured BOLD amplitudes in the four types of stimulus blocks (represented by four color traces for each person in Fig. To assess the effects of top-down attention and visual awareness on BOLD responses within the targeted monocular region in V1. This arrangement induced a transparent percept where the two stimuli spatially overlapped but the central portion (6° in diameter) of the target motion grating was constantly visible. shown on two oblique slices for one participant from a separate localization scan. Stimulus design and the location and BOLD response in the targeted monocular region. calcarine sulcus.sciencemag. In two out of four participants. (D) Portions of V1. compare cyan and magenta traces in Fig. Performance of all participants was above 90% correct for the target visibility task and above 75% correct for the letter detection 830 11 NOVEMBER 2011 VOL 334 Downloaded from www. CS. we found a highly significant effect of attention regardless of visibility conditions (P < 0. In an additional scan session. 1. A and C). 2011 s Tscore .05. dorsal V1. In the “visible stimulus on November 13. and in one participant. There was no consistent effect of visibility on BOLD responses across the four participants. Supplementary psychophysical results indicate that inattentional blindness was less likely to occur in our stimulus condition. We set the ratio of the two types of stimuli within a block to 14:2 so that we could reliably direct the participant’s attention to the target when necessary and in the meantime maintain the high contrast in target visibility to measure the potential difference in BOLD response between the two blocks. the visible stimulus in the attention to nontarget condition evoked a slightly higher BOLD response than the invisible stimulus (P < 0. we localized the portion of V1 corresponding to the monocular target (Fig. left. the participants were capable of reporting the existence of the target when interviewed after they performed the character detection task (SOM). V1d. Slice positions on a sagittal slice and anatomical landmarks on the two oblique slices are shown on the left. in the “attention to nontarget block.” the person was instructed to report the visibility of the target (a two-alternative forced choice between visible and invisible) for 16 consecutive stimulus presentations within a block.sciencemag. (E) Time courses of average BOLD responses in the targeted monocular region [red pixels in (D)] to the counterphasing checkerboard (red trace) and to the ring-shaped dynamic Mondrian pattern presented either to the dominant eye (blue) or nondominant eye (cyan). compare red and blue traces in Fig. the task instruction was signaled by the color of fixation: Red characters instructed the participant to report the visibility of the target motion grating [as exemplified in (A)]. 1C).001) for all four participants studied. and SOM). V1v. Conversely. (C) Visible and invisible stimulus blocks: Catch stimuli were introduced so that the participant could reliably maintain attention to the target when instructed. and green pixels indicate the region activated by the Mondrian pattern. During the experiment. whereas the target motion grating was presented to the nondominant eye. (B) The invisible stimulus: The dynamic Mondrian pattern was presented to the dominant eye. L. 2. In the “attention to target block. (A) The visible stimulus: The dynamic Mondrian pattern and target motion grating were both presented to the nondominant eye and were interleaved in successive video frames (at 60 Hz).” the person was required to detect a given character in a rapidly presented series of characters at the center of fixation (SOM). 2C).

Reddy. L. K. Psychol. 11. Science and Technology grant no. J. Acad. 27. 6. E. indicate that neural processes of top-down attention may extend to lower levels in the visual hierarchy as compared to the neural correlates of visual awareness. 2. 14. R. Logothetis. These. 140 (1991). The four time courses in each panel (for each of four participants) were obtained from the target visible with attention to target block (magenta). Cortex 14. 24. whereas numerous functional magnetic resonance imaging studies report a strong attentional modulation on the BOLD signal in human V1 (8–13). D. Natl. attention and awareness are intimately interrelated. 96. Tajima for early discussion and model simulation related to the project. 46. accepted 28 September 2011 10. a lesion in V1 would also heavily affect this area by removing a large portion of its afferent input. P. Sci. Braun. 28. Sports. C. Soc. Cortex 15. We have also conducted a multivariate pattern analysis. I. Transcranial magnetic stimulation (TMS) studies suggest that the feedback activity from the middle temporal area to V1 is crucial for visual awareness of TMS-induced motion phosphenes (27) and motion stimuli (28). 9596 (2002).).S. Watanabe. Acad. Engel. 96. Trends Cogn. R. 26. Neurosci. Previous studies have shown a large and significant awareness modulation on the BOLD signal in both human and monkey V1 (17. L. We thank D. S. Heeger. 8. Leopold. Rajimehr. Neurosci. U. Previous findings claim a functional role of V1 in awareness. Neurosci. Ungerleider. Lavie. 27. Heeger. Maruya. 611 (2004). do not completely rule out the involvement of V1 in visual awareness (see SOM for a hybrid conceptual model providing a possible interpretation of our results under the assumption that V1 activity is not modulated by awareness). 7. Tsuchiya. As in the case of blindsight. VanRullen.S. downstream areas can be equally affected by the consequences of TMS application to V1. Naccache. J. too. 18. Acknowledgments: This work was supported by Japanese Ministry of Education. Eckhorn. Nat. M. 416 (2002). E. C. Culture. Materials and Methods SOM Text Figs. Li. A.. Natl. Wilken. Percept. Sci. 1 (1998). P. 11. Julesz. Oxford. Nature 411. 103. Our results suggest that this is actually the case. Trends Neurosci. C. Reddy. seem to contradict our results. Neurosci.sciencemag. H. A. Nat. 4. Proc. but the claim that feedback activity to V1 is a necessary condition for awareness does not necessarily point to V1 as an area for neural modulation by the contents of conscious percept. Nat. G. J. and the previously reported awareness modulation on the BOLD signal in V1 is likely to be an artifact caused by the concurrent attentional modulation.S. or using neural dynamics instead of firing rates (such as synchronization) that differ from hemodynamic measurements and conventional neural recordings. J. J. N. The extent of the modulation of visual awareness on neuronal activity in V1 is crucial because V1 lies at the bottom of the cortical visual hierarchy. 1736 (2005). V. H. Voinescu for help with data collection and S. A similar twist exists for attention. A. 20. www. 2. N. Vis. Seiffert. 22. 300 (2004). Natl. on November 13. U. D. A. Blindsight (Oxford Univ. U. Koch. Tong. A.sciencemag. 14. Philos. Vis. Walsh. 17507 (2006). A. 668 (2005). Boynton. Neurosci. Logothetis. 8. A. 15). no. 751 (1999). A. target invisible with attention to target block (cyan). N. C. Logothetis. C. Koch. Annu. A. Dehaene. Cereb. 25. 549 (1996). Nat. Silvanto. M. G. Cook. DeYoe. Sci. 26). Proc. B.A. P. Gail. Reddy. Press. Proc. Brinksmeyer. 1193 (2008). SCIENCE VOL 334 www. 95. 21. M. 19. Sci. 11. Vis. M. R. 13. because attention was not thoroughly controlled in these previous studies. target visible with attention to nontarget location block (red). Vis. A. it should be emphasized that our current conclusions. Natl.1203161 11 NOVEMBER 2011 831 Downloaded from www. 18. are needed to further clarify the involvement of V1 in visual awareness. 10. 23. Proc. The phenomenon of blindsight (namely. Walsh. Acad. R. References and Notes 1. Somers. and target invisible with attention to nontarget block (blue). Nat. (A to D) Time courses of averaged BOLD responses and 95% confidence intervals in the targeted monocular region. M.A. F. A. Blake. 3. P. Watanabe et al. Psychophys. Nature 379. K. J. Proc. Koch. 3314 (1999). 1986). 195 (2001). Pascual-Leone. Polonsky. 5. 370 (1999). De Weerd. R. Maier et al. Sci. U.. D. Rev. N. Cowey. Leopold. Science 292. This is in line with recent psychophysical findings that top-down attention may affect neural representations of invisible stimuli. However. Kastner. Pinsk. Supporting Online Material Fig.S. L. N. Reynolds. 106 (2004). S. V. 60.sciencemag. 2. Vision Res. U. 16. 99. F. Sci. K. P. whereas single-unit studies have failed to detect robust perception-locked changes (16.REPORTS reported effects might be caused by the differences in involuntary eye movements among stimulustask conditions (SOM). 5. J. 1096 (2005). Koch. 8. F. L. Acad. The previously observed discrepancy between single-unit activity and BOLD signal in V1 in visual awareness experiments could be simply explained by attentional modulation. Tootell. Tsuchiya. L. Desimone. However. J. Weiskrantz. R. Dale. 1063 (2002). Cereb. single-unit studies claim only modest attentional effects in monkey V1 (14. C. 510 (2001). Neuron 22. S1 to S10 References 21 January 2011. Sci. J.S. Stoerig. 19–21). 17. article 7 (2008). S. E. Maier. Braun. Leopold. S. P. without adequate control. Maunsell. B 357. This is indeed a major experimental complication because. B. Koch. Wilke.W.A. D. 9. resulting in aftereffect (2) and priming (3). A. L. D. 21). Trans. Martínez et al. The increase of the BOLD signal with attention in V1 agrees with the previous literature (8–13).A. 15. J. T. the manifestation of residual visual processing despite the total loss of visual awareness) caused by lesions in V1 suggests a role for V1 in awareness (25. 1663 (1999). 13. 1153 (2000). J. if we assume the existence of a hypothetical area downstream of V1 as a neural correlate of awareness. H. 2336 (2006). as revealed by univariate BOLD effects. the results from all participants showed a near-chance classification between visible and invisible stimuli for both attentional conditions (SOM). 434 (2004). H. Blandin. A. based solely on BOLD measurements. Perona. L. Watanabe. A. 2011 . the results regarding awareness in our study challenge the currently established view that the BOLD signal in V1 correlates robustly with the contents of percept. E. Brefczynski. 16 (2007). Gandhi. J. N. A. J. R. London Ser. 364 (1999). Acad. 1702215 (M. K. using nonbiased and fine-scale neuronal measurement techniques that can capture the modulation in local circuits in V1 (such as specific neuronal subtypes). A. Montaser-Kouhsari. 11489 (1998).A. 11. Chelazzi.. The current results. Future efforts. However. 4. which seems to be immune to the problem of attentional confounds. D. Natl. respectively.1126/science. 12. Neurosci.

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