Elsevier

NeuroImage

Volume 51, Issue 2, June 2010, Pages 828-834
NeuroImage

The role of early visual cortex (V1/V2) in conscious and unconscious visual perception

https://doi.org/10.1016/j.neuroimage.2010.02.042Get rights and content

Abstract

A “late” period of activity in striate cortex (V1) in response to extrastriate feedback has been proposed to act as a marker of visual awareness. It is not clear, however, whether such recurrent activity is associated exclusively with aware perception or whether it is necessary also for unaware visual processing. We investigated the role of the “late” V1 activity in both aware and unaware visual motion perception. Participants were asked to make a forced-choice direction discrimination judgment on a coherently moving random-dot display and additionally rate their subjective awareness of the stimulus. Transcranial magnetic stimulation (TMS) was applied over the early visual cortex (V1/V2) either 20, 40, 60, 80, or 100 ms after motion offset. Visual awareness was impaired at an “early” (20 ms) and a “late” (60 ms) stimulation time window. Participants' forced-choice direction discrimination performance on “unaware” trials was above chance in No TMS baseline condition. Importantly, this performance was impaired by TMS over V1/V2 at the “late” time window. In a second experiment we show that the critical time window of V5/MT falls between the “early” and “late” time windows of V1/V2 activity. The results indicate that recurrent extrastriate-V1 activity is necessary for both aware and unaware perception.

Introduction

The role of striate cortex (V1) in visual awareness has been the subject of much debate (Pollen, 1999, Pollen, 2003, Pollen, 2008, Lamme, 2001, Block, 2005). In particular, a “late” period of V1 activity, in response to feedback from extrastriate areas, has been associated with visual awareness (Lamme, 2001, Lamme, 2006, Lamme and Roelfsema, 2000). Consistent with this view, single-cell recordings in macaques have shown that the “late” period of V1 activity correlates with the animal's perceptual report (Super et al., 2001), and functional neuroimaging with human subjects has revealed that activity in the early visual cortex is predictive of whether or not a subject consciously perceives a visual stimulus (Ress and Heeger, 2003, Kamitani and Tong, 2005).

Much of the causal evidence for this view has come from transcranial magnetic stimulation (TMS) studies. In a seminal study, Cowey and Walsh (2000) attempted to induce phosphenes from intact extrastriate regions of the blindsight subject GY who had suffered an almost complete destruction of his left V1. He was able to perceive TMS-induced phosphenes induced from the contralesional hemisphere, but not when intact extrastriate regions in his ipsilesional hemisphere were stimulated, demonstrating that the integrity of V1 is critical for aware experience of V5/MT activation.

This view has been supported by studies conducted in neurologically normal observers. Pascual-Leone and Walsh (2001) applied TMS over V5/MT to elicit moving phosphenes and found that a subsequent TMS pulse delivered over the early visual cortex degraded the sensation of phosphene motion. The timing of the disruptive effect of V1 TMS implied that V5/MT activation reaches awareness via V1 (see also Silvanto et al., 2005a). Feedback connections have also been shown to be necessary for aware perception of visually presented motion (Silvanto et al., 2005b). This was achieved by applying TMS over either V1/V2 or V5/MT at different time windows after the presentation of a moving stimulus to trace the information flow that gives rise to visual awareness. The results showed two critical periods of V1 activity, one preceding and another postdating the V5/MT critical period, suggesting that although V5/MT obtains visual information through V1 feedforward activity, backprojections from V5/MT to V1 remain critical for awareness of motion. These observations occur in the context of a substantial electrophysiological literature on the modulatory impact of extrastriate feedback on neural responses in V1 (e.g., Hupé et al., 1998, Hupé et al., 2001, Zipser et al., 1996, Lamme et al., 1998).

Although these findings demonstrate the importance of recurrent activity and V1 in aware visual perception, whether the “late” period of V1 activity is unique to aware perception or rather a general feature of visual cortical information processing (mediating both aware and unaware perception) is not known. This is because the literature is unclear on the necessity of the “late” period of V1 activity in conditions in which the subjects are able to unconsciously detect target stimuli of which they are unaware (assessed for example using forced-choice paradigms). Boyer et al. (2005) found above chance forced-choice discrimination of colour and orientation of unaware stimuli when TMS was applied over V1, suggesting that V1 is not necessary for unaware processing of these features. However, this result on its own does not imply a lack of V1 involvement in unaware perception; it is possible that forced-choice discrimination was impaired by TMS even though it remained above chance. Boyer et al. (2005) did not include a baseline condition against which the performance in the V1 TMS condition could be compared to and it is therefore unclear whether TMS affected unaware perception. Sack et al. (2009) reported recently that TMS to early visual cortex 60, 80, and 100 ms after prime onset impaired response priming produced by arrow symbols. As response priming for such symbols should proceed normally without awareness (Vorberg et al., 2003), this result suggests that early visual cortex is necessary for unaware perception, although it remains unclear whether feedforward or recurrent processing was measured by Sack et al. (2009).

In the present study we addressed this issue by using TMS to investigate the necessity of the “late” V1 activity for both aware and unaware visual perception. This was accomplished by the use of both subjective and objective measures of motion perception on each trial. Specifically, subjects were asked to provide a rating of their subjective perceptual experience of visually presented motion stimuli and in addition to perform a forced-choice direction discrimination task on the same stimuli. If the “late” period of V1 activity is unique to visual awareness, the application of TMS during this stage should weaken subjective experience of motion but leave forced-choice discrimination performance on unaware trials unaffected. In contrast, if the “late” V1 activity reflects a general principle of visual cortical information processing, TMS should disrupt performance in both tasks. In Experiment 2, we investigated the time course of the critical role of the motion selective area V5/MT in motion perception. In order to confirm that the “late” V1 activity reflected feedback from V5/MT, the critical period of V5/MT activity should fall between the “early” and “late” periods of V1 activity.

Section snippets

Participants

Sixteen participants (nine males; mean age = 22.8 years, range: 20–26), all of whom were naive to the objective of the study, took part in Experiment 1. The study was approved by the local ethics committee of the Hospital District of Southwest Finland, undertaken with the understanding and written consent of each subject, and conducted in accordance with the Declaration of Helsinki.

Stimuli

The stimuli were presented on a 19″ monitor with 1024 × 768 pixel resolution. The viewing distance was 150 cm. Each trial

Baseline (No TMS) condition

In the baseline condition, participants reported having no awareness of motion (rating = 0) on 10% (SD = 9), no awareness of motion direction (rating = 1) on 17% (SD = 10), sensing the motion direction without actually seeing it (rating = 2) on 33% (SD = 13), and consciously seeing the motion direction (rating = 3) on 39% (SD = 26) of trials. Analysis of accuracy on these baseline trials (including only the 10 participants who had more than 15 observations for each rating) showed that, as one would expect,

Discussion

The objective of this study was to investigate whether the “late” period of early visual cortical (V1/V2) activity is necessary specifically for aware visual perception or whether it is necessary also for unaware perception. Consistent with a previous study (Silvanto et al., 2005b) we found two periods of V1/V2 activity (an “early” one at 20 ms and a “late” one at 60 ms after stimulus offset) associated with the awareness of motion. The “early” time window is likely to reflect the role of V1 in

Acknowledgments

This work was supported by the Academy of Finland [grant number 125175]. We thank Teemu Laine for technical help.

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