Unconscious Touch Perception After Disruption of the Primary Somatosensory Cortex.

Brain damage or disruption to the primary visual cortex sometimes produces blindsight, a striking condition in which patients lose the ability to consciously detect visual information yet retain the ability to discriminate some attributes without awareness. Although there have been few demonstrations of somatosensory equivalents of blindsight, the lesions that produce "numbsense," in which patients can make accurate guesses about tactile information without awareness, have been rare and localized to different regions of the brain. Despite transient loss of tactile awareness in the contralateral hand after transcranial magnetic stimulation (TMS) of the primary somatosensory cortex but not TMS of a control site, 12 participants (six female) reliably performed at above-chance levels on a localization task. These results demonstrating TMS-induced numbsense implicate a parallel somatosensory pathway that processes the location of touch in the absence of awareness and highlight the importance of primary sensory cortices for conscious perception.

Ipsilesional perceptual deficits in hemispatial neglect: Case reports.

Hemispatial neglect, usually after right hemisphere lesions, is characterized by contralesional deficits in attention and perception. However, little is known about impairments of perceptual processing in the ipsilesional region of visual space (the right visual field for right hemisphere lesions). In two right hemisphere neglect patients, we used a metacontrast masking paradigm to characterize systematic spatial and temporal visual processing deficits in the ipsilesional right visual field. The presence of a visual mask caused the neglect patients to miss targets in ipsilesional space, even when a mask was presented as long as 1.5 sec after the target and in a different spatial position. These prolonged and spatially extended masking effects were not measured in age-matched healthy controls or in two control patients with hemianopsia but without neglect. The results show that perceptual processing is distorted and delayed in a region of the visual field that has been thought to be unaffected - the ipsilesional hemifield in patients with neglect.

Visual Modulation of Resting State α Oscillations.

Once thought to simply reflect passive cortical idling, recent studies have demonstrated that α oscillations play a causal role in cognition and perception. However, whether and how cognitive or sensory processes modulate various components of the α rhythm is poorly understood. Sensory input and resting states were manipulated in human subjects while electroencephalography (EEG) activity was recorded in three conditions: eyes-open fixating on a visual stimulus, eyes-open without visual input (darkness), and eyes-closed without visual input (darkness). We show that α power and peak frequency increase when visual input is reduced compared to the eyes open, fixating condition. These results suggest that increases in α power reflect a shift from an exteroceptive to interoceptive state and that increases in peak frequency following restricted visual input (darkness) may reflect increased sampling of the external environment in order to detect stimuli. They further demonstrate how sensory information modulates α and the importance of selecting an appropriate resting condition in studies of α.

Competitive Frontoparietal Interactions Mediate Implicit Inferences.

Frequent experience with regularities in our environment allows us to use predictive information to guide our decision process. However, contingencies in our environment are not always explicitly present and sometimes need to be inferred. Heretofore, it remained unknown how predictive information guides decision-making when explicit knowledge is absent and how the brain shapes such implicit inferences. In the present experiment, 17 human participants (9 females) performed a discrimination task in which a target stimulus was preceded by a predictive cue. Critically, participants had no explicit knowledge that some of the cues signaled an upcoming target, allowing us to investigate how implicit inferences emerge and guide decision-making. Despite unawareness of the cue-target contingencies, participants were able to use implicit information to improve performance. Concurrent EEG recordings demonstrate that implicit inferences rely upon interactions between internally and externally oriented networks, whereby prefrontal regions inhibit parietal cortex under internal implicit control.SIGNIFICANCE STATEMENT Regularities in our environment can guide our behavior providing information about upcoming events. Interestingly, such predictive information does not need to be explicitly represented to effectively guide our decision process. Here, we show how the brain engages in such real-world "data mining" and how implicit inferences emerge. We used a contingency cueing task and demonstrated that implicit inferences influenced responses to subsequent targets despite a lack of awareness of cue-target contingencies. Further, we show that these implicit inferences emerge through interactions between internally and externally oriented neural networks. The current results highlight the importance of prefrontal processes in transforming external events into predictive internalized models of the world.

Alpha Oscillations and Feedback Processing in Visual Cortex for Conscious Perception.

Variability in perception between individuals may be a consequence of different inherent neural processing speeds. To assess whether alpha oscillations systematically reflect a feedback pacing mechanism for cortical processing during visual perception, comparisons were made between alpha oscillations, visual suppression from TMS, visual evoked responses, and metacontrast masking. Peak alpha oscillation frequencies, measured through scalp EEG recordings, significantly correlated with the optimum latencies for visual suppression from TMS of early visual cortex. Individuals with shorter alpha periods (i.e., higher peak alpha frequencies) processed visual information faster than those with longer alpha periods (i.e., lower peak alpha frequencies). Moreover, peak alpha oscillation periods and optimum TMS visual suppression latencies predicted the latencies of late but not early visual evoked responses. Together, these findings demonstrate an important role of alpha oscillatory and late feedback activity in visual cortex for conscious perception. They also show that the timing for visual awareness varies across individuals, depending on the pace of one's endogenous oscillatory cycling frequency.

Dissociations of conscious and unconscious perception in TMS-induced blindsight.

As with some patients with primary visual cortex (V1) damage, transcranial magnetic stimulation (TMS) over V1 reliably induces blindsight, whereby observers can correctly discriminate the attributes of visual stimuli despite being unable to detect them. This TMS-induced blindsight has been demonstrated to reflect a form of unconscious vision that relies upon different neural pathways than with conscious vision. However, the timing of the neural processes mediating TMS-induced blindsight has been unclear, especially when considering suggestions that TMS interferes with feedback processes to V1 that mediate conscious visual perception. To better elucidate the neural mechanisms that give rise to blindsight, we tested TMS-induced blindsight for the orientation of visual stimuli across a range of stimulus onset asynchronies (SOAs) to assess how different latencies of visual cortex disruption, relative to a visual stimulus, affect detection rates and forced-choice discrimination accuracy. At all TMS latencies, including at SOAs with substantial visual suppression from TMS, discrimination performance was significantly above-chance, demonstrating the consistency of TMS-induced blindsight. Crucially, we observed two windows of maximum visual suppression from TMS at SOAs between 65 and 105 ms, but consistent above-chance discrimination performance accuracy across these windows. However, at longer SOAs, detection and discrimination covaried, suggesting a dependency of discrimination performance on detection only when detection rates exceed threshold levels of normal vision. Taken together, these results indicate that unconscious discrimination occurs independently of detection, including at TMS intervals that optimally interfere with conscious visual perception. They further suggest that forced-choice discrimination is less dependent on feedback processes to V1 than visual awareness and that TMS-induced blindsight is not the same as near-threshold vision.

Effects of canonical color, luminance, and orientation on sustained inattentional blindness for scenes.

Whether scene gist perception occurs automatically and unconsciously has been the subject of much debate. In addition to demonstrating a new method that adapts the Mack and Rock (1998) inattentional blindness cross procedure to allow for sustained inattentional blindness over a large number of trials, we report evidence from a series of experiments that shows that canonical scene features reduce inattentional blindness to scenes by facilitating the extraction of scene gist. When attentional demands are high, the combination of canonical color, canonical luminance, and canonical orientation reduces rates of inattentional blindness. However, when attentional demands are reduced, canonical features are independently sufficient to facilitate gist extraction and to capture attention. These results demonstrate that canonical color, canonical luminance, and canonical orientation all contribute to scene gist perception, and that when attentional demands are high, only highly canonical stimuli are sufficient to capture attention.

Retinal and visual cortex distance from transcranial magnetic stimulation of the vertex affects phosphene perception.

Recent studies claim that the perception of flashes of light (i.e., phosphenes) can be induced by stimulation of higher visual areas, including parietal cortex, suggesting a critical role of these regions in generating visual percepts. In this study, we show that transcranial magnetic stimulation (TMS) of even the vertex can induce phosphenes, but that their neural origins are likely to be a consequence of current spread into visual areas (e.g., retina or visual cortex). After vertex stimulation, subjects with smaller head circumferences-for whom the distances from the coil to retina and visual cortex are smaller-report a two-fold increase in perceiving phosphenes. In contrast, both smaller and larger headed individuals perceived phosphenes equivalently and on nearly all trials following TMS of early visual cortex. These results demonstrate a critical role of early visual areas but not higher ones in generating visual perceptions. These findings further suggest that phosphenes perceived from TMS of the vertex or parietal cortex arise from induced activity in the retina or nearby early visual cortex and warn against the use of the vertex as a control site for TMS experiments of visual perception.

Transcranial magnetic stimulation to visual cortex induces suboptimal introspection.

Blindsight patients with damage to the visual cortex can discriminate objects but report no conscious visual experience. This provides an intriguing opportunity to allow the study of subjective awareness in isolation from objective performance capacity. However, blindsight is rare, so one promising way to induce the effect in neurologically intact observers is to apply transcranial magnetic stimulation (TMS) to the visual cortex. Here, we used a recently-developed criterion-free method to conclusively rule out an important alternative interpretation of TMS-induced performance without awareness: that TMS-induced blindsight may be just due to conservative reporting biases for conscious perception. Critically, using this criterion-free paradigm we have previously shown that introspective judgments were optimal even under visual masking. However, here under TMS, observers were suboptimal, as if they were metacognitively blind to the visual disturbances caused by TMS. We argue that metacognitive judgments depend on observers' internal statistical models of their own perceptual systems, and introspective suboptimality arises when external perturbations abruptly make those models invalid - a phenomenon that may also be happening in actual blindsight.

Who's afraid of response bias?

Response bias (or criterion) contamination is insidious in studies of consciousness: that observers report they do not see a stimulus may not mean they have absolutely no subjective experience; they may be giving such reports in relative terms in the context of other stimuli. Bias-free signal detection theoretic measures provide an excellent method for avoiding response bias confounds, and many researchers correctly adopt this approach. However, here we discuss how a fixation on avoiding criterion effects can also be misleading and detrimental to fruitful inquiry. In a recent paper, Balsdon and Azzopardi (Absolute and relative blindsight. Consciousness and Cognition 2015; 32:79-91.) claimed that contamination by response bias led to flawed findings in a previous report of "relative blindsight". We argue that their criticisms are unfounded. They mistakenly assumed that others were trying (and failing) to apply their preferred methods to remove bias, when there was no such intention. They also dismissed meaningful findings because of their dependence on criterion, but such dismissal is problematic: many real effects necessarily depend on criterion. Unfortunately, these issues are technically tedious, and we discuss how they may have confused others to misapply psychophysical metrics and to draw questionable conclusions about the nature of TMS (transcranial magnetic stimulation)-induced blindsight. We conclude by discussing the conceptual importance of criterion effects in studies of conscious awareness: we need to treat them carefully, but not to avoid them without thinking.

Perceptual overloading reveals illusory contour perception without awareness of the inducers.

Unconscious perception is frequently examined by restricting visual input (e.g., using short stimulus durations followed by masking) to prevent that information from entering visual awareness. Failures to demonstrate perception without awareness may thus be a consequence of this restricted input rather than of limitations in unconscious perception. Here, we demonstrate a novel method that circumvents these significant drawbacks inherent in other methods. Using this new perceptual overloading technique (POT), in which stimuli are repeatedly presented in alternation with a stream of variable masks, we demonstrate illusory contour perception and modal completion even when subjects are completely unaware of the inducing elements. In addition to demonstrating a powerful new method to study consciousness by effectively gating robust visual input from visual awareness, we show that more complex contextual effects, previously considered to be a privilege only of conscious vision, can occur without awareness.

Action-specific disruption of perceptual confidence.

Theoretical models of perception assume that confidence is related to the quality or strength of sensory processing. Counter to this intuitive view, we showed in the present research that the motor system also contributes to judgments of perceptual confidence. In two experiments, we used transcranial magnetic stimulation (TMS) to manipulate response-specific representations in the premotor cortex, selectively disrupting postresponse confidence in visual discrimination judgments. Specifically, stimulation of the motor representation associated with the unchosen response reduced confidence in correct responses, thereby reducing metacognitive capacity without changing visual discrimination performance. Effects of TMS on confidence were observed when stimulation was applied both before and after the response occurred, which suggests that confidence depends on late-stage metacognitive processes. These results place constraints on models of perceptual confidence and metacognition by revealing that action-specific information in the premotor cortex contributes to perceptual confidence.

EEG-microstate dependent emergence of perceptual awareness.

We investigated whether the differences in perceptual awareness for stimuli at the threshold of awareness can arise from different global brain states before stimulus onset indexed by the EEG microstate. We used a metacontrast backward masking paradigm in which subjects had to discriminate between two weak stimuli and obtained measures of accuracy and awareness while their EEG was recorded from 256 channels. Comparing targets that were correctly identified with and without awareness allowed us to contrast differences in awareness while keeping performance constant for identical physical stimuli. Two distinct pre-stimulus scalp potential fields (microstate maps) dissociated correct identification with and without awareness, and their estimated intracranial generators were stronger in primary visual cortex before correct identification without awareness. This difference in activity cannot be explained by differences in alpha power or phase which were less reliably linked with differential pre-stimulus activation of primary visual cortex. Our results shed a new light on the function of pre-stimulus activity in early visual cortex in visual awareness and emphasize the importance of trial-by-trials analysis of the spatial configuration of the scalp potential field identified with multichannel EEG.

Dynamics of alpha control: preparatory suppression of posterior alpha oscillations by frontal modulators revealed with combined EEG and event-related optical signal.

We investigated the dynamics of brain processes facilitating conscious experience of external stimuli. Previously, we proposed that alpha (8-12 Hz) oscillations, which fluctuate with both sustained and directed attention, represent a pulsed inhibition of ongoing sensory brain activity. Here we tested the prediction that inhibitory alpha oscillations in visual cortex are modulated by top-down signals from frontoparietal attention networks. We measured modulations in phase-coherent alpha oscillations from superficial frontal, parietal, and occipital cortices using the event-related optical signal (EROS), a measure of neuronal activity affording high spatiotemporal resolution, along with concurrently recorded EEG, while participants performed a visual target detection task. The pretarget alpha oscillations measured with EEG and EROS from posterior areas were larger for subsequently undetected targets, supporting alpha's inhibitory role. Using EROS, we localized brain correlates of these awareness-related alpha oscillations measured at the scalp to the cuneus and precuneus. Crucially, EROS alpha suppression correlated with posterior EEG alpha power across participants. Sorting the EROS data based on EEG alpha power quartiles to investigate alpha modulators revealed that suppression of posterior alpha was preceded by increased activity in regions of the dorsal attention network and decreased activity in regions of the cingulo-opercular network. Cross-correlations revealed the temporal dynamics of activity within these preparatory networks before posterior alpha modulation. The novel combination of EEG and EROS afforded localization of the sources and correlates of alpha oscillations and their temporal relationships, supporting our proposal that top-down control from attention networks modulates both posterior alpha and awareness of visual stimuli.

Amodal completion of unconsciously presented objects.

In the visual environment, objects often appear behind occluding surfaces, yet they are automatically and effortlessly perceived as complete. Here, we examined whether visually occluded objects that are presented below the threshold of awareness are amodally completed. We used a priming paradigm in which participants responded to consciously perceived targets that were preceded by unconsciously presented primes. In two experiments, we show that discrimination responses to targets were faster when they were preceded by congruent shapes, regardless of whether these shapes were intact and complete or occluded by a horizontal bar. This priming effect was not produced by a partial match in features, since the occluded primes did not facilitate responses to targets that shared local features (Experiment 1) or contained only the object features that remained visible after occlusion (Experiment 2). These results show that objects presented below the threshold of awareness can be amodally completed and provide compelling evidence that unconscious processing occurs to a greater extent than previously considered.

The phase of prestimulus alpha oscillations affects tactile perception.

Previous studies have shown that neural oscillations in the 8- to 12-Hz range influence sensory perception. In the current study, we examined whether both the power and phase of these mu/alpha oscillations predict successful conscious tactile perception. Near-threshold tactile stimuli were applied to the left hand while electroencephalographic (EEG) activity was recorded over the contralateral right somatosensory cortex. We found a significant inverted U-shaped relationship between prestimulus mu/alpha power and detection rate, suggesting that there is an intermediate level of alpha power that is optimal for tactile perception. We also found a significant difference in phase angle concentration at stimulus onset that predicted whether the upcoming tactile stimulus was perceived or missed. As has been shown in the visual system, these findings suggest that these mu/alpha oscillations measured over somatosensory areas exert a strong inhibitory control on tactile perception and that pulsed inhibition by these oscillations shapes the state of brain activity necessary for conscious perception. They further suggest that these common phasic processing mechanisms across different sensory modalities and brain regions may reflect a common underlying encoding principle in perceptual processing that leads to momentary windows of perceptual awareness.

Direct control of visual perception with phase-specific modulation of posterior parietal cortex.

We examined the causal relationship between the phase of alpha oscillations (9-12 Hz) and conscious visual perception using rhythmic TMS (rTMS) while simultaneously recording EEG activity. rTMS of posterior parietal cortex at an alpha frequency (10 Hz), but not occipital or sham rTMS, both entrained the phase of subsequent alpha oscillatory activity and produced a phase-dependent change on subsequent visual perception, with lower discrimination accuracy for targets presented at one phase of the alpha oscillatory waveform than for targets presented at the opposite phase. By extrinsically manipulating the phase of alpha before stimulus presentation, we provide direct evidence that the neural circuitry in the parietal cortex involved with generating alpha oscillations plays a causal role in determining whether or not a visual stimulus is successfully perceived.

Synesthesia: a colorful word with a touching sound?

Synesthesia is a fairly common condition in which individuals experience atypical responses (such as color experiences) in association with certain types of stimuli (such as non-colored letters). Although synesthesia has been described for centuries, only very recently has there been an explosive growth of systematic scientific examinations of this condition. In this article, we review and critically evaluate current methods for both assessing synesthesia and examining its psychological basis, including the "test-retest" procedure, online battery assessments, and behavioral experiments. We highlight the limitations of these methods for understanding the nature of this complex condition and propose potential solutions to address some of these limitations. We also provide a set of markers that aid in distinguishing synesthesia from other closely related psychological phenomena.