Does TMS on V3 block conscious visual perception?

Primary visual cortex (V1) and extrastriate V2 are necessary for the emergence of visual consciousness, but the effects of involvement of extrastriate V3 on visual consciousness is unclear. The objective of this study was to examine the causal role of V3 in visual consciousness in humans. We combined neuronavigated transcranial magnetic stimulation (TMS) with a computational model of the TMS-induced electric field to test whether or not the intact processing of visual input in V3, like in V1 and V2, is necessary for conscious visual perception. We targeted the stimulation both to V2 and to V3. If TMS of V3 blocks conscious visual perception of stimuli, then activation in V3 is a causally necessary prerequisite for conscious perception of stimuli. According to the alternative hypothesis, TMS of V3 will not block the conscious visual perception of stimuli, because the pathways from V1 to the higher cortical areas that go around V3 provide sufficient visual input for the emergence of conscious visual perception. The results showed that TMS interfered with conscious perception of features, detection of stimulus presence and the ability to discriminate the letter stimuli both when TMS was targeted either to V3 or to V2. For the conscious detection of stimulus presence, the effect was significantly stronger when V2 was stimulated than when V3 was stimulated. The results of the present study suggest that in addition to the primary visual cortex and V2, also V3 causally contributes to the generation of the most basic form of visual consciousness. Importantly, the results also indicate that V3 is necessary for visual perception in general, not only for visual consciousness.

TMS-EEG reveals hemispheric asymmetries in top-down influences of posterior intraparietal cortex on behavior and visual event-related potentials.

Clinical data and behavioral studies using transcranial magnetic stimulation (TMS) suggest right-hemisphere dominance for top-down modulation of visual processing in humans. We used concurrent TMS-EEG to directly test for hemispheric differences in causal influences of the right and left intraparietal cortex on visual event-related potentials (ERPs). We stimulated the left and right posterior part of intraparietal sulcus (IPS1) while the participants were viewing and rating the visibility of bilaterally presented Gabor patches. Subjective visibility ratings showed that TMS of right IPS shifted the visibility toward the right hemifield, while TMS of left IPS did not have any behavioral effect. TMS of right IPS, but not left one, reduced the amplitude of posterior N1 potential, 180-220ms after stimulus-onset. The attenuation of N1 occurred bilaterally over the posterior areas of both hemispheres. Consistent with previous TMS-fMRI studies, this finding suggests that the right IPS has top-down control on the neural processing in visual cortex. As N1 most probably reflects reactivation of early visual areas, the current findings support the view that the posterior parietal cortex in the right hemisphere amplifies recurrent interactions in ventral visual areas during the time-window that is critical for conscious perception.

Transcranial magnetic stimulation of early visual cortex suppresses conscious representations in a dichotomous manner without gradually decreasing their precision.

Transcranial magnetic stimulation (TMS) of early visual cortex can suppresses visual perception at early stages of processing. The suppression can be measured both with objective forced-choice tasks and with subjective ratings of visual awareness, but there is lack of objective evidence on how and whether the TMS influences the quality of representations. Does TMS decrease the precision of representations in graded manner, or does it lead to dichotomous, "all-or-nothing" suppression. We resolved this question by using a continuous measure of the perceptual error: the observers had to perceive the orientation of a target (Landort-C) and to adjust the orientation of a probe to match that of the target. Mixture modeling was applied to estimate the probability of guess trials and the standard deviation of the non-guess trials. TMS delivered 60-150 ms after stimulus-onset influenced only the guessing rate, whereas the standard deviation (i.e., precision) was not affected. This suggests that TMS suppressed representations dichotomously without affecting their precision. The guessing probability correlated with subjective visibility ratings, suggesting that it measured visual awareness. In a control experiment, manipulation of the stimulus contrast affected the standard deviation of the errors, indicating that contrast has a gradual influence on the precision of representations. The findings suggest that TMS of early visual cortex suppresses perception in dichotomous manner by decreasing the signal-to-noise ratio by increasing the noise level, whereas reduction of the signal level (i.e., contrast) decreases the precision of representations.

Different Electrophysiological Correlates of Visual Awareness for Detection and Identification.

Detecting the presence of an object is a different process than identifying the object as a particular object. This difference has not been taken into account in designing experiments on the neural correlates of consciousness. We compared the electrophysiological correlates of conscious detection and identification directly by measuring ERPs while participants performed either a task only requiring the conscious detection of the stimulus or a higher-level task requiring its conscious identification. Behavioral results showed that, even if the stimulus was consciously detected, it was not necessarily identified. A posterior electrophysiological signature 200-300 msec after stimulus onset was sensitive for conscious detection but not for conscious identification, which correlated with a later widespread activity. Thus, we found behavioral and neural evidence for elementary visual experiences, which are not yet enriched with higher-level knowledge. The search for the mechanisms of consciousness should focus on the early elementary phenomenal experiences to avoid the confounding effects of higher-level processes.

Subjective visual awareness emerges prior to P3.

Studies on the neural basis of visual awareness, the subjective experience of seeing, have found several potential neural correlates of visual awareness. Some of them may not directly correlate with awareness but with post-perceptual processes, such as reporting one's awareness of the stimulus. We dissociated potential electrophysiological correlates of visual awareness from those occurring during response selection and thus co-occurring with post-perceptual processing. The participants performed two GO-NOGO conditions. In the aware-GO condition they responded with a key press when they were aware of the stimulus and withheld responding when they were unaware of it. In the unaware-GO condition they withheld responding when they were aware and responded when they were not aware of the stimulus. Thus, event-related potentials could be measured to aware and unaware trials when responding was required and when not required. The results revealed that the N200 amplitude (180-280 ms) over the occipital and posterior temporal cortex was enhanced in aware trials as compared with trials without awareness. This effect (visual awareness negativity, VAN) did not depend on responding. The amplitude of P3 (350-450 ms) also was enhanced in aware trials as compared with unaware trials. In addition, the amplitudes in the P3 time window depended on responding: they were greater when awareness was mapped to GO-response than when not, suggesting that P3 reflects post-perceptual processing, that is, it occurs after awareness has emerged. These findings support theories of visual awareness that assume a relatively early onset of visual awareness before P3.

Subjective characteristics of TMS-induced phosphenes originating in human V1 and V2.

One way to study the neural correlates of visual consciousness is to localize the cortical areas whose stimulation generates subjective visual sensations, called phosphenes. While there is support for the view that the stimulation of several different visual areas in the occipital lobe may produce phosphenes, it is not clear what the contribution of each area is. Here, we studied the roles of the primary visual cortex (V1) and the adjacent area V2 in eliciting phosphenes by using functional magnetic resonance imaging-guided transcranial magnetic stimulation (TMS) combined with spherical modeling of the TMS-induced electric field. Reports of the subjective visual features of phosphenes were systematically collected and analyzed. We found that selective stimulation of V1 and V2 are equally capable of generating phosphenes, as demonstrated by comparable phosphene thresholds and similar characteristics of phosphene shape, color, and texture. However, the phosphenes induced by V1 stimulation were systematically perceived as brighter than the phosphenes induced by the stimulation of V2. Thus, these results suggest that V1 and V2 have a similar capability to produce conscious percepts. Nevertheless, V1 and V2 contribute differently to brightness: neural activation originating in V1 generates a more intense sensation of brightness than similar activation originating in V2.

Retinotopic maps, spatial tuning, and locations of human visual areas in surface coordinates characterized with multifocal and blocked FMRI designs.

The localization of visual areas in the human cortex is typically based on mapping the retinotopic organization with functional magnetic resonance imaging (fMRI). The most common approach is to encode the response phase for a slowly moving visual stimulus and to present the result on an individual's reconstructed cortical surface. The main aims of this study were to develop complementary general linear model (GLM)-based retinotopic mapping methods and to characterize the inter-individual variability of the visual area positions on the cortical surface. We studied 15 subjects with two methods: a 24-region multifocal checkerboard stimulus and a blocked presentation of object stimuli at different visual field locations. The retinotopic maps were based on weighted averaging of the GLM parameter estimates for the stimulus regions. In addition to localizing visual areas, both methods could be used to localize multiple retinotopic regions-of-interest. The two methods yielded consistent retinotopic maps in the visual areas V1, V2, V3, hV4, and V3AB. In the higher-level areas IPS0, VO1, LO1, LO2, TO1, and TO2, retinotopy could only be mapped with the blocked stimulus presentation. The gradual widening of spatial tuning and an increase in the responses to stimuli in the ipsilateral visual field along the hierarchy of visual areas likely reflected the increase in the average receptive field size. Finally, after registration to Freesurfer's surface-based atlas of the human cerebral cortex, we calculated the mean and variability of the visual area positions in the spherical surface-based coordinate system and generated probability maps of the visual areas on the average cortical surface. The inter-individual variability in the area locations decreased when the midpoints were calculated along the spherical cortical surface compared with volumetric coordinates. These results can facilitate both analysis of individual functional anatomy and comparisons of visual cortex topology across studies.

Neuronavigated transcranial magnetic stimulation suggests that area V2 is necessary for visual awareness.

The primary visual cortex (V1) has been shown to be critical for visual awareness, but the importance of other low-level visual areas has remained unclear. To clarify the role of human cortical area V2 in visual awareness, we applied transcranial magnetic stimulation (TMS) over V2 while participants were carrying out a visual discrimination task and rating their subjective awareness. Individual retinotopic maps and modelling of the TMS-induced electric field in V1, V2 and V3d ensured that the electric field was at or under the phosphene threshold level in V1 and V3d, whereas in V2 it was at the higher suppressive level. As earlier shown for the V1, our results imply that also V2 is necessary for conscious visual experience. Visual awareness of stimulus presence was completely suppressed when the TMS pulse was delivered 44-84 ms after the onset of visual stimulus. Visual discrimination and awareness of stimulus features was impaired when the TMS pulse was delivered 44-104 ms after the visual stimulus onset. These results suggest that visual awareness cannot be generated without an intact V2.

Is selective primary visual cortex stimulation achievable with TMS?

The primary visual cortex (V1) has been the target of stimulation in a number of transcranial magnetic stimulation (TMS) studies. In this study, we estimated the actual sites of stimulation by modeling the cortical location of the TMS-induced electric field when participants reported visual phosphenes or scotomas. First, individual retinotopic areas were identified by multifocal functional magnetic resonance imaging (mffMRI). Second, during the TMS stimulation, the cortical stimulation sites were derived from electric field modeling. When an external anatomical landmark for V1 was used (2 cm above inion), the cortical stimulation landed in various functional areas in different individuals, the dorsal V2 being the most affected area at the group level. When V1 was specifically targeted based on the individual mffMRI data, V1 could be selectively stimulated in half of the participants. In the rest, the selective stimulation of V1 was obstructed by the intermediate position of the dorsal V2. We conclude that the selective stimulation of V1 is possible only if V1 happens to be favorably located in the individual anatomy. Selective and successful targeting of TMS pulses to V1 requires MRI-navigated stimulation, selection of participants and coil positions based on detailed retinotopic maps of individual functional anatomy, and computational modeling of the TMS-induced electric field distribution in the visual cortex. It remains to be resolved whether even more selective stimulation of V1 could be achieved by adjusting the coil orientation according to sulcal orientation of the target site.

Unconscious and conscious processing of color rely on activity in early visual cortex: a TMS study.

Chromatic information is processed by the visual system both at an unconscious level and at a level that results in conscious perception of color. It remains unclear whether both conscious and unconscious processing of chromatic information depend on activity in the early visual cortex or whether unconscious chromatic processing can also rely on other neural mechanisms. In this study, the contribution of early visual cortex activity to conscious and unconscious chromatic processing was studied using single-pulse TMS in three time windows 40-100 msec after stimulus onset in three conditions: conscious color recognition, forced-choice discrimination of consciously invisible color, and unconscious color priming. We found that conscious perception and both measures of unconscious processing of chromatic information depended on activity in early visual cortex 70-100 msec after stimulus presentation. Unconscious forced-choice discrimination was above chance only when participants reported perceiving some stimulus features (but not color).

Recurrent processing in V1/V2 contributes to categorization of natural scenes.

Humans are able to categorize complex natural scenes very rapidly and effortlessly, which has led to an assumption that such ultra-rapid categorization is driven by feedforward activation of ventral brain areas. However, recent accounts of visual perception stress the role of recurrent interactions that start rapidly after the activation of V1. To study whether or not recurrent processes play a causal role in categorization, we applied fMRI-guided transcranial magnetic stimulation on early visual cortex (V1/V2) and lateral occipital cortex (LO) while the participants categorized natural images as containing animals or not. The results showed that V1/V2 contributed to categorization speed and to subjective perception during a long activity period before and after the contribution of LO had started. This pattern of results suggests that recurrent interactions in visual cortex between areas along the ventral stream and striate cortex play a causal role in categorization and perception of natural scenes.

Transcranial magnetic stimulation of early visual cortex interferes with subjective visual awareness and objective forced-choice performance.

In order to study whether there exist a period of activity in the human early visual cortex that contributes exclusively to visual awareness, we applied transcranial magnetic stimulation (TMS) over the early visual cortex and measured subjective visual awareness during visual forced-choice symbol or orientation discrimination tasks. TMS produced one dip in awareness 60-120 ms after stimulus onset, while forced-choice orientation discrimination was suppressed between 60 and 90 ms and symbol discrimination between 60 and 120 ms. Thus, a time window specific to visual awareness was found only in the orientation condition at 120 ms. The results imply that both conscious and unconscious perception depend on activity in early visual areas. On the basis of previous estimates of neural processing speed, we suggest that the late part of the activity period most likely involve local extrastriate-striate interactions which provide the contents for visual awareness but are not themselves sufficient for awareness to arise.