Task relevance differentially shapes ventral visual stream sensitivity to visible and invisible faces

Neuroscience of Consciousness, 2016, 1–8 doi: 10.1093/nc/niw021 Research article Task relevance differentially shapes ventral visual stream sensitivity to visible and invisible faces  Brain and Consciousness Group (ENS, EHESS, CNRS), Ecole Normale Supérieure—PSL Research University, Paris, France; 2Section for Cognitive Systems, Technical University of Denmark, Lyngby, Denmark; 3Science division, Psychology, New York University—Abu Dhabi, United Arab Emirates; 4Department of Psychology, New York University, New York, USA; 5Danish Research Centre for Magnetic Resonance, Copenhagen University ^trière University Hospital, Hospital, Hvidovre, Denmark; 6Centre de NeuroImagerie de Recherche, Pitié-Salpe Paris, France; 7Department of Experimental Psychology, University of Oxford, Oxford, UK 1 *Correspondence address: Ecole Normale Supérieure, 29 rue d’Ulm, 75005, Paris, France. Tel: þ33 1 44 32 26 22; E-mail: Abstract Top-down modulations of the visual cortex can be driven by task relevance. Yet, several accounts propose that the perceptual inferences underlying conscious recognition involve similar top-down modulations of sensory responses. Studying the pure impact of task relevance on sensory responses requires dissociating it from the top-down influences underlying conscious recognition. Here, using visual masking to abolish perceptual consciousness in humans, we report that functional magnetic resonance imaging (fMRI) responses to invisible faces in the fusiform gyrus are enhanced when they are taskrelevant, but suppressed when they are task-irrelevant compared to other object categories. Under conscious perceptual conditions, task-related modulations were also present but drastically reduced, with visible faces always eliciting greater activity in the fusiform gyrus compared to other object categories. Thus, task relevance crucially shapes the sensitivity of fusiform regions to face stimuli, leading from enhancement to suppression of neural activity when the top-down influences accruing from conscious recognition are prevented. Key words: FFA; fMRI; subliminal perception; attention Neuronal activity in visual cortex reflect the interplay between bottom-up processing of sensory inputs and top-down influences from higher-order regions such as the prefrontal cortex (Corbetta and Shulman 2002; Gilbert and Li 2013). One major source of top-down modulation reflects the current task relevance, promoting sensory representations that are behaviourally relevant at the expense of competing irrelevant information (Desimone and Duncan 1995; Peelen et al. 2009; Peters et al. 2012). However, characterizing the impact of task relevance on visual regions remains challenging, because the mere recognition of a stimulus, regardless of task relevance, involves perceptual inferences that also influence sensory responses via top-down modulations (Mumford 1992; Ullman 1995; Friston 2005; Gilbert and Sigman 2007). Specifically, whenever bottom-up signals accumulate enough to cross a threshold, top-down mechanisms are triggered, allowing for the amplification and maintenance of sensory information in visual cortex and the concomitant elaboration of a conscious perceptual representation (Dehaene and Changeux 2011). Since perceptual inference might prompt participants to focus on task-irrelevant information (e.g. a familiar face while searching for alternative objects), previous studies may have, thus, unwittingly C The Author 2016. Published by Oxford University Press. V This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact 1 Sid Kouider,1,2,3 Antoine Barbot,1,4 Kristoffer H. Madsen,2,5 Stéphane Lehericy,6 and Christopher Summerfield7 2 | Kouider et al. confounded these two distinct sources of top-down influences (O’Craven et al. 1999; Summerfield et al. 2006). A potential solution to this issue consists in studying how task relevance shapes sensory responses during non-conscious processing stages, prior to the elaboration of a conscious percept. Non-conscious processing occurs when sensory signals are rendered invisible, usually through visual masking, but continue inducing influences at both neural and behavioural levels (Breitmeyer and Ogmen 2006; Kouider and Dehaene 2007), without exciting the re-entrant processing characteristics of conscious perception (Lamme and Roelfsema 2000; Dehaene and Changeux 2011). For instance, the fusiform face area (FFA)—an extrastriate region within the ventral visual stream with neurons preferentially tuned to faces (Kanwisher et al. 1997)—remains responsive to faces even when they are rendered fully invisible by masking (Morris et al. 2007; Kouider et al. 2009; Fahrenfort et al. 2012). Yet, it remains unclear whether FFA responses to invisible faces can be biased by task relevance. To address this issue, we measured fMRI BOLD responses in the FFA to faces and non-face objects that were either visible or invisible, and either task-relevant or task-distracting (Fig. 1). Participants made category-specific detection judgements by pressing a button only for faces in face detection blocks, and only for alternative objects (e.g. watches) in alternative detection blocks. Thus, face stimuli and alternative objects were in turn task-relevant or task-distracting across blocks. This design allowed us comparing whether FFA responses to invisible stimuli are exclusively influenced by stimulus category (i.e. stronger response for faces regardless of the task relevance) or rather dependant on task relevance (i.e. stronger response for faces only when this category is task-relevant). In the latter case, the use of an additional control category (e.g. flowers) that was never task-relevant throughout the experiment allowed us to test whether task-distracting faces are simply ignored (i.e. filtering of FFA responses) or actually inhibited (i.e. suppression of FFA responses; Fig. 2). Methods Subjects A total of 20 healthy volunteers (12 females, age 24 6 5 years, all university students) gave written consent to participate in the study. All volunteers were right-handed, had normal or correct-to-normal vision and were in good health, with no history of psychiatric or neurological illness. The protocol of this study was approved by the local ethical committee (CPP 71-07, Pitié-Salpétrière, Paris, France). Stimuli The stimuli were greyscale photographs of 180 faces, 180 flowers and 180 watches serving as critical stimuli, in addition to 200 filler stimuli equally balanced across 10 categories (balls, burgers, cars, cups, donuts, fruits, guitars, hats, snails, wheels). Stimuli across the different categories were matched for image size, as well as for average luminance and contr (...truncated)