The neural processes generating visual phenomenal consciousness: ERP and neuronavigated brain stimulation studies

One of the greatest conundrums to the contemporary science is the relation between consciousness and brain activity, and one of the specifi c questions is how neural activity can generate vivid subjective experiences. Studies focusing on visual consciousness have become essential in solving the empirical questions of consciousness. Th e main aim of this thesis is to clarify the relation between visual consciousness and the neural and electrophysiological processes of the brain. By applying electroencephalography and functional magnetic resonance image-guided transcranial magnetic stimulation (TMS), we investigated the links between conscious perception and attention, the temporal evolution of visual consciousness during stimulus processing, the causal roles of primary visual cortex (V1), visual area 2 (V2) and lateral occipital cortex (LO) in the generation of visual consciousness and also the methodological issues concerning the accuracy of targeting TMS to V1. Th e results showed that the fi rst eff ects of visual consciousness on electrophysiological responses (about 140 ms aft er the stimulus-onset) appeared earlier than the eff ects of selective attention, and also in the unattended condition, suggesting that visual consciousness and selective attention are two independent phenomena which have distinct underlying neural mechanisms. In addition, while it is well known that V1 is necessary for visual awareness, the results of the present thesis suggest that also the abutting visual area V2 is a prerequisite for conscious perception. In our studies, the activation in V2 was necessary for the conscious perception of change in contrast for a shorter period of time than in the case of more detailed conscious perception. We also found that TMS in LO suppressed the conscious perception of object shape when TMS was delivered in two distinct time windows, the latter corresponding with the timing of the ERPs related to the conscious perception of coherent object shape. Th e result supports the view that LO is crucial in conscious perception of object coherency and is likely to be directly involved in the generation of visual consciousness. Furthermore, we found that visual sensations, or phosphenes, elicited by the TMS of V1 were brighter than identically induced phosphenes arising from V2. Th ese fi ndings demonstrate that V1 contributes more to the generation of the sensation of brightness than does V2. Th e results also suggest that top-down activation from V2 to V1 is probably associated with phosphene generation. The results of the methodological study imply that when a commonly used landmark (2 cm above the inion) is used in targeting TMS to V1, the TMS-induced electric fi eld is likely to be highest in dorsal V2. When V1 was targeted according to the individual retinotopic data, the electric fi eld was highest in V1 only in half of the participants. Th is result suggests that if the objective is to study the role of V1 with TMS methodology, at least functional maps of V1 and V2 should be applied with computational model of the TMS-induced electric fi eld in V1 and V2. Finally, the results of this thesis imply that diff erent features of attention contribute diff erently to visual consciousness, and thus, the theoretical model which is built up of the relationship between visual consciousness and attention should acknowledge these diff erences. Future studies should also explore the possibility that visual consciousness consists of several processing stages, each of which have their distinct underlying neural mechanisms.Tajunnallisuus ja sen suhde aivojen neuraalisiin tapahtumiin on yksi tieteen suurimmista ratkaisemattomista kysymyksistä. Tyypillisesti tajunnallisuudella viitataan fenomenaaliseen tajuntaan eli yksilön elämykselliseen ja välittömään kokemukseen tietystä sisällöstä. Tajunnallinen näkeminen eli visuaalinen tajunta on noussut keskiöön tajunnan neuraalisten korrelaattien tutkimuksessa. Tarkastelen tässä tutkimuksessa aivokuoren aktivaation ja visuaalisen tajunnan välistä korrelaatio- ja kausaalisuhdetta elektroenkefalografi an (EEG), toiminnallisten magneettikuvien avulla ohjatun transkraniaalisen magneettistimulaation (TMS) sekä TMS:n indusoiman sähkökentän mallinnuksen avulla. Erityisesti tavoitteena on tarkentaa näönvaraisen tajunnan ja tarkkaavaisuuden välistä suhdetta, tajunnan ajallista kehittymistä, ensimmäisen näköaivokuoren alueen (alue V1), alueen V2 ja lateraalisen näköaivokuoren (LO-alue) roolia visuaalisessa tajunnassa. Väitöskirja koostuu viidestä osatutkimuksesta. Tulokset osoittivat, että varhaisimmat visuaalisen tajunnan vaikutukset tapahtumasidonnaisiin herätevasteisiin (ERP) tulivat esiin noin 140 ms ärsykkeen esittämisen jälkeen ja selvästi ennen valikoivan tarkkaavaisuuden vaikutusta sekä riippumatta valikoivan tarkkaavaisuuden vaikutuksesta. Tulos viittaa siihen, että visuaalisen tajunnan ja valikoivan tarkkaavaisuuden taustalla on erilliset neuraaliset prosessit. Alueen V1 tiedetään olevan välttämätön normaalille näönvaraiselle tajunnalliselle kokemukselle, mutta kolmannen osatutkimuksen tulokset tukevat oletusta, että myös viereinen alue V2 on välttämätön normaalille visuaaliselle tajunnalle. Lisäksi havaittiin, että aktivaatio alueella V2 oli välttämätöntä visuaalisen ärsykkeen yksityiskohtien prosessoinnille pidempään kuin tajunnallisuudelle ärsykkeen läsnäolosta. LO-alueen stimulointi TMS:lla taas ehkäisi tajunnallisen kokemuksen tutusta objektista kahdessa erillisessä aikaikkunassa, joista jälkimmäisen ajoitus korreloi tajuntaan liittyvän tyypillisen ERP-vasteen ajoituksen kanssa. Tutkimustulos tuo tukea näkemykselle jonka mukaan LO-alueen aktivaatio liittyy suoraan niihin prosesseihin, jotka generoivat tajunnallisen havainnon objektista. Okkipitaalilohkon TMS- ja sähköstimuloinnin tiedetään aiheuttavan subjektiivisia valoaistimuksia eli fosfeeneja. Tutkimuksessa havaittiin, että alueen V1 ja alueen V2 stimuloinnin avulla tuotetut fosfeenit ovat keskenään hyvin samankaltaisia muodon, värin sekä koon osalta, mutta alueen V1 stimuloinnissa tuotetut fosfeenit olivat kaikilla tutkittavilla kirkkaampia kuin alueen V2 stimuloinnilla tuotetut fosfeenit. Menetelmällisessä tutkimuksessa havaittiin, että vaikka TMS-pulssi oli suunnattu alueelle V1 toiminnallisten magneettikuvien tai kallon muodon mukaan, oli todennäköisempää, että indusoitu sähkökenttä oli ollut voimakkaampi alueen V2 päällä. Toisaalta toisen osatutkimuksen tulokset osoittivat, että joillekin tutkittaville alueen V1 TMS-stimulaatio oli mahdollista, kun erityistä huomiota kiinnitettiin retinotooppisten edustusalueiden valitsemiseen ja hyödynnettiin sähkökentänmallinnusmenetelmää. Kokonaisuudessaan tämän tutkimuksen tulokset viittaavat siihen, että eri tarkkaavaisuuden muodot vaikuttavat eri tavoin näönvaraiseen tajuntaan, ja näin ollen, teoreettisen mallin visuaalisen tajunnan ja tarkkaavaisuuden välisestä suhteesta tulisi ottaa huomioon nämä erot. Tulevissa tutkimuksissa tulisi myös selvittää mahdollisuutta, jonka mukaan näönvarainen tajunta koostuu useista prosessointi tasosta, joista jokaisella on erilliset hermostolliset perustansa.Siirretty Doriast

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, 180-220 ms 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

Neural correlates of subjective awareness for natural scene categorization of color photographs and line-drawings

It remains controversial whether visual awareness is correlated with early activation indicated by VAN (visual awareness negativity), as the recurrent process hypothesis theory proposes, or with later activation indicated by P3 or LP (late positive), as suggested by global workspace theories. To address this issue, a backward masking task was adopted, in which participants were first asked to categorize natural scenes of color photographs and line-drawings and then to rate the clarity of their visual experience on a perceptual awareness scale (PAS). The interstimulus interval (ISI) between the scene and the mask was manipulated. The behavioral results showed that categorization accuracy increased with PAS ratings for both color photographs and line-drawings, with no difference in accuracy between the two types of images for each rating, indicating that the experience rating reflected visibility. Importantly, the ERP results revealed that for correct trials, the early posterior N1 and anterior P2 components changed with the PAS ratings for color photographs, but did not vary with the PAS ratings for line-drawings, indicating that the N1 and P2 do not always correlate with subjective visual awareness. Moreover, for both types of images, the anterior N2 and posterior VAN changed with the PAS ratings in a linear way, while the LP changed with the PAS ratings in a nonlinear way,suggesting that these components relate to different types of subjective awareness. The results reconcile the apparently contradictory predictions of different theories and help to resolve the current debate on neural correlates of visual awareness

Why is “blindsight” blind? A new perspective on primary visual cortex, recurrent activity and visual awareness

The neuropsychological phenomenon of blindsight has been taken to suggest that the primary visual cortex (V1) plays a unique role in visual awareness, and that extrastriate activation needs to be fed back to V1 in order for the content of that activation to be consciously perceived. The aim of this review is to evaluate this theoretical framework and to revisit its key tenets. Firstly, is blindsight truly a dissociation of awareness and visual detection? Secondly, is there sufficient evidence to rule out the possibility that the loss of awareness resulting from a V1 lesion simply reflects reduced extrastriate responsiveness, rather than a unique role of V1 in conscious experience? Evaluation of these arguments and the empirical evidence leads to the conclusion that the loss of phenomenal awareness in blindsight may not be due to feedback activity in V1 being the hallmark awareness. On the basis of existing literature, an alternative explanation of blindsight is proposed. In this view, visual awareness is a “global” cognitive function as its hallmark is the availability of information to a large number of perceptual and cognitive systems; this requires inter-areal long-range synchronous oscillatory activity. For these oscillations to arise, a specific temporal profile of neuronal activity is required, which is established through recurrent feedback activity involving V1 and the extrastriate cortex. When V1 is lesioned, the loss of recurrent activity prevents inter-areal networks on the basis of oscillatory activity. However, as limited amount of input can reach extrastriate cortex and some extrastriate neuronal selectivity is preserved, computations involving comparison of neural firing rates within a cortical area remain possible. This enables “local” read-out from specific brain regions, allowing for the detection and discrimination of basic visual attributes. Thus blindsight is blind due to lack of “global” long-range synchrony, and it functions via “local” neural readout from extrastriate areas

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

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

a b s t r a c t 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

Recurrent Processing in V1/V2 Contributes ot 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

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.</p

Group-average eccentricity and polar angle maps.

<p>The retinotopic maps obtained with the object mapping were averaged across the 15 subjects using the cortical surface-based coordinate system. Nodes with data from less than three subjects were omitted from the maps. The visual area borders were defined based on group-averages of the individuals' visual area labels brought into the average surface.</p