Rapid recurrent processing gates awareness in primary visual cortex

Abstract

Visual awareness has been proposed to depend on recurrent processing in early visual cortex areas including the primary visual cortex (V1). Here, we address this hypothesis with high spatiotemporal resolution magnetoencephalographic recordings in subjects performing a substitution masking paradigm. Neural activity reflecting awareness is assessed by directly comparing the neuromagnetic response elicited by effectively and ineffectively masked targets after the proportion of trials leading to masking was individually adjusted to match the proportion of trials without masking. This revealed a modulation of recurrent activity in the primary visual cortex rapidly after the onset of the feedforward sweep of processing in striate and extrastriate areas but significantly before the onset of attention-dependent recurrent modulations in V1. Our data provide direct support for the notion that (i) recurrent processing in V1 correlates with visual awareness and (ii) that attention and awareness involve distinct recurrent processing operations.magnetoencephalography ͉ visual attention ͉ visual awareness T here is considerable evidence suggesting that attention influences activity in early visual cortex areas, including the primary visual cortex via feedback-driven modulations (1-4). Data from single cell recordings in the monkey have revealed that such feedback may operate via selective rate enhancements in V1 that label the segmentation of relevant input for priority for further processing (5, 6). Conversely, there is evidence suggesting that attentional feedback operates by suppressing irrelevant input, thereby increasing the relative prominence of relevant input representations in V1 (7).Beyond its undoubted role for attentional selection, feedback processing from extrastriate to primary visual cortex has also been implicated as an important factor for mediating visual awareness (6,(8)(9)(10)(11). Empirical evidence for this claim has been provided by a number of experimental approaches. While recording from V1 neurons in the macaque, Lamme et al. (12) observed that backward masking by texture patterns did not influence the initial feedforward activity elicited by the figure but caused a suppression of the delayed figure-ground modulation of neural firing, the latter being assumed to be mediated by feedback connections. Furthermore, Super et al. (13) could show that the delayed modulation reflecting figure-ground segregation was reduced in V1 when the monkey failed to identify the figure-ground stimulus.Ress and colleagues (14, 15) report related observations with fMRI in human observers. They observed that better discrimination performance at visual detection thresholds correlated with a blood oxygenation level dependent (BOLD) response enhancement in primary visual cortex (14). This was the case even when subjectively perceived stimuli were physically absent (15). Although Ress and Heeger (15) discuss an explanation in terms of bottom-up fluctuations of sensory processing in V1, they also entertain the possibility tha...

Subjective visibility depends on level of processing

“…Additionally, an fMRI study with the geometrical shape stimuli and a similar subjective visibility scale confirmed that graded perceptual reports from participants reflect genuine intermediate brain states rather than response artefacts (Christensen, Ramsøy, Lund, Madsen, & Rowe, 2006). Several other studies have presented stimuli that are processed early on in the processing hierarchy, and found recurrent processing between posterior brain regions (Boehler, Schoenfeld, Heinze, & Hopf, 2008;Fahrenfort, Scholte, & Lamme, 2008) to be associated with conscious perception. Such findings have led Lamme (2006), Lamme (2010) to develop a graded account of conscious visual perception, which we will call the Recurrent Processing Hypothesis (RPH): higher and lower visual regions engaging in increasing recurrent interactions subtend the gradual increase of awareness of a stimulus, perhaps by promoting increased stability of the corresponding neural activation patterns.…”

Recurrent Neural Processing and Somatosensory Awareness

“…So far, evidence for the notion that perceptual consciousness arises through recurrent loops of activity between brain areas (Lamme, 2000(Lamme, , 2006 has been primarily limited to studies of vision (Pascual-Leone and Walsh, 2001;Ro et al, 2003;Silvanto et al, 2005;Boehler et al, 2008;Fahrenfort et al, 2008), with an exception of a recent DCM/EEG study in which auditory stimuli were delivered to patients with severe disorders of consciousness (Boly et al, 2011). Our findings allow for a generalization of the recurrent processing hypothesis to the somatosensory modality, suggesting that recurrent activity between regions involved in stimulus processing might be a general mechanism underlying perceptual awareness.…”

“…Parallel to studies on basic perceptual processes, recurrent processing has gained popularity as a candidate mechanism underlying perceptual consciousness, with evidence ranging from studies using transcranial magnetic stimulation-induced phosphenes (Pascual-Leone and Walsh, 2001), to visual masking (Ro et al, 2003;Boehler et al, 2008;Fahrenfort et al, 2008), motion detection tasks (Silvanto et al, 2005; but see , and effective connectivity analyses in patients with consciousness disorders (Boly et al, 2011). As a result, several influential views on consciousness treat recurrent activity as a condition necessary (Dehaene et al, 2006;Tononi and Koch, 2008) or even sufficient (Lamme, 2000(Lamme, , 2006 for perceptual awareness.…”

Synchronization of fronto-parietal beta and theta networks as a signature of visual awareness in neglect

“…Fronto-parietal networks have also been demonstrated to subserve executive control and working memory (Egner et al, 2008;Bressler and Menon, 2010;Menon, 2013;Rottschy et al, 2012Rottschy et al, , 2013, with prominent activations found in the right hemisphere (Hardwick et al, 2013). Hence, pathologies of these networks or their long-distance connections can critically impair conscious visual perception independently of (van Boxtel et al, 2010;Sumner et al, 2006;Tsuchiya and Koch, 2008;Boehler et al, 2008) or in addition to deficits of attention and central executive networks (Chica et al, 2013). However, the role of fronto-parietal networks for deficient conscious perception, a key symptom in neglect, has remained less well explored.…”