Distinct ventral stream and prefrontal cortex representational dynamics during sustained conscious visual perception.

Instances of sustained stationary sensory input are ubiquitous. However, previous work focused almost exclusively on transient onset responses. This presents a critical challenge for neural theories of consciousness, which should account for the full temporal extent of experience. To address this question, we use intracranial recordings from ten human patients with epilepsy to view diverse images of multiple durations. We reveal that, in sensory regions, despite dramatic changes in activation magnitude, the distributed representation of categories and exemplars remains sustained and stable. In contrast, in frontoparietal regions, we find transient content representation at stimulus onset. Our results highlight the connection between the anatomical and temporal correlates of experience. To the extent perception is sustained, it may rely on sensory representations and to the extent perception is discrete, centered on perceptual updating, it may rely on frontoparietal representations.

Error monitoring when no errors are possible: Arbitrary free-choice decisions invoke error monitoring processes.

Some decisions make a difference, but most are arbitrary and inconsequential, like which of several identical new pairs of socks should I wear? Healthy people swiftly make such decisions even with no rational reasons to rely on. In fact, arbitrary decisions have been suggested as demonstrating "free will". However, several clinical populations and some healthy individuals have significant difficulties in making such arbitrary decisions. Here, we investigate the mechanisms involved in arbitrary picking decisions. We show that these decisions, arguably based on a whim, are subject to similar control mechanisms as reasoned decisions. Specifically, error-related negativity (ERN) brain response is elicited in the EEG following change of intention, without an external definition of error, and motor activity in the non-responding hand resembles actual errors both by its muscle EMG temporal dynamics and by the lateralized readiness potential (LRP) pattern. This provides new directions in understanding decision-making and its deficits.

Distinct interacting cortical networks for stimulus-response and repetition-suppression.

Non-invasive studies consider the initial neural stimulus response (SR) and repetition suppression (RS) - the decreased response to repeated sensory stimuli - as engaging the same neurons. That is, RS is a suppression of the SR. We challenge this conjecture using electrocorticographic (ECoG) recordings with high spatial resolution in ten patients listening to task-irrelevant trains of auditory stimuli. SR and RS were indexed by high-frequency activity (HFA) across temporal, parietal, and frontal cortices. HFASR and HFARS were temporally and spatially distinct, with HFARS emerging later than HFASR and showing only a limited spatial intersection with HFASR: most HFASR sites did not demonstrate HFARS, and HFARS was found where no HFASR could be recorded. ß activity was enhanced in HFARS compared to HFASR cortical sites. θ activity was enhanced in HFASR compared to HFARS sites. Furthermore, HFASR sites propagated information to HFARS sites via transient θ:ß phase-phase coupling. In contrast to predictive coding (PC) accounts our results indicate that HFASR and HFARS are functionally linked but have minimal spatial overlap. HFASR might enable stable and rapid perception of environmental stimuli across extended temporal intervals. In contrast HFARS might support efficient generation of an internal model based on stimulus history.

Neuroscientific Evidence for Processing Without Awareness.

The extent to which we are affected by perceptual input of which we are unaware is widely debated. By measuring neural responses to sensory stimulation, neuroscientific data could complement behavioral results with valuable evidence. Here we review neuroscientific findings of processing of high-level information, as well as interactions with attention and memory. Although the results are mixed, we find initial support for processing object categories and words, possibly to the semantic level, as well as emotional expressions. Robust neural evidence for face individuation and integration of sentences or scenes is lacking. Attention affects the processing of stimuli that are not consciously perceived, and such stimuli may exogenously but not endogenously capture attention when relevant, and be maintained in memory over time. Sources of inconsistency in the literature include variability in control for awareness as well as individual differences, calling for future studies that adopt stricter measures of awareness and probe multiple processes within subjects.

Context Sensitivity across Multiple Time scales with a Flexible Frequency Bandwidth.

Everyday auditory streams are complex, including spectro-temporal content that varies at multiple timescales. Using EEG, we investigated the sensitivity of human auditory cortex to the content of past stimulation in unattended sequences of equiprobable tones. In 3 experiments including 82 participants overall, we found that neural responses measured at different latencies after stimulus onset were sensitive to frequency intervals computed over distinct timescales. Importantly, early responses were sensitive to a longer history of stimulation than later responses. To account for these results, we tested a model consisting of neural populations with frequency-specific but broad tuning that undergo adaptation with exponential recovery. We found that the coexistence of neural populations with distinct recovery rates can explain our results. Furthermore, the adaptation bandwidth of these populations depended on spectral context-it was wider when the stimulation sequence had a wider frequency range. Our results provide electrophysiological evidence as well as a possible mechanistic explanation for dynamic and multiscale context-dependent auditory processing in the human cortex.

Brain-based concealed memory detection is driven mainly by orientation to salient items.

In the pursuit of new methods for concealed memory detection, event-related potential components (ERP) have been placed at the forefront of research. No method, however, is scientifically complete without a theory and the present study therefore aimed to unravel the cognitive processes underlying these ERPs (i.e., orienting and arousal inhibition). This was accomplished by using a Concealed Information Test (CIT) in which participants were once motivated to conceal and once motivated to reveal their identity. The results showed a similarly strong P3 CIT effect in the two motivational conditions, which was enhanced for high salience compared to low salience identity items. Similar results were observed when using a multivariate machine-learning algorithm - suggesting that brain-based concealed memory detection is driven mainly by orientation to salient stimuli, rather than by arousal inhibition. In addition, the algorithm, trained and tested on the ERPs of different identity items, achieved detection rates exceeding those achieved by the P3. This implies that CIT researchers and practitioners could potentially rely on the entire ERP waveform instead of a-priori selecting separate components. Together these results enrich current understanding of the mechanisms underlying neurophysiological responding to concealed information and pave the way for novel and powerful algorithms which could be used in real-life forensic investigations.

Face Selective Neural Activity: Comparisons Between Fixed and Free Viewing.

Event Related Potentials (ERPs) are widely used to study category-selective EEG responses to visual stimuli, such as the face-selective N170 component. Typically, this is done by flashing stimuli at the point of static gaze fixation. While allowing for good experimental control, these paradigms ignore the dynamic role of eye-movements in natural vision. Fixation-related potentials (FRPs), obtained using simultaneous EEG and eye-tracking, overcome this limitation. Various studies have used FRPs to study processes such as lexical processing, target detection and attention allocation. The goal of this study was to carefully compare face-sensitive activity time-locked to an abrupt stimulus onset at fixation, with that time-locked to a self-generated fixation on a stimulus. Twelve participants participated in three experimental conditions: Free-viewing (FRPs), Cued-viewing (FRPs) and Control (ERPs). We used a multiple regression approach to disentangle overlapping activity components. Our results show that the N170 face-effect is evident for the first fixation on a stimulus, whether it follows a self-generated saccade or stimulus appearance at fixation point. The N170 face-effect has similar topography across viewing conditions, but there were major differences within each stimulus category. We ascribe these differences to an overlap of the fixation-related lambda response and the N170. We tested the plausibility of this account using dipole simulations. Finally, the N170 exhibits category-specific adaptation in free viewing. This study establishes the comparability of the free-viewing N170 face-effect with the classic event-related effect, while highlighting the importance of accounting for eye-movement related effects.

Resting-state EEG topographies: Reliable and sensitive signatures of unilateral spatial neglect.

Theoretical advances in the neurosciences are leading to the development of an increasing number of proposed interventions for the enhancement of functional recovery after brain damage. Integration of these novel approaches in clinical practice depends on the availability of reliable, simple, and sensitive biomarkers of impairment level and extent of recovery, to enable an informed clinical-decision process. However, the neuropsychological tests currently in use do not tap into the complex neural re-organization process that occurs after brain insult and its modulation by treatment. Here we show that topographical analysis of resting-state electroencephalography (rsEEG) patterns using singular value decomposition (SVD) could be used to capture these processes. In two groups of subacute stroke patients, we show reliable detection of deviant neurophysiological patterns over repeated measurement sessions on separate days. These patterns generalized across patients groups. Additionally, they maintained a significant association with ipsilesional attention bias, discriminating patients with spatial neglect of different severity levels. The sensitivity and reliability of these rsEEG topographical analyses support their use as a tool for monitoring natural and treatment-induced recovery in the rehabilitation process.

Effect of Aging on Change of Intention.

Decision making often requires making arbitrary choices ("picking") between alternatives that make no difference to the agent, that are equally desirable, or when the potential reward is unknown. Using event-related potentials we tested the effect of age on this common type of decision making. We compared two age groups: ages 18-25, and ages 41-67 on a masked-priming paradigm while recording EEG and EMG. Participants pressed a right or left button following either an instructive arrow cue or a neutral free-choice picking cue, both preceded by a masked arrow or neutral prime. The prime affected the behavior on the Instructed and the Free-choice picking conditions both in the younger and older groups. Moreover, electrophysiological "Change of Intention" (ChoI) was observed via lateralized readiness potential (LRP) in both age groups - the polarity of the LRP indicated first preparation to move the primed hand and then preparation to move the other hand. However, the older participants were more conservative in responding to the instructive cue, exhibiting a speed-accuracy trade-off, with slower response times, less errors in incongruent trials, and reduced probability of EMG activity in the non-responding hand. Additionally, "Change of Intention" was observed in both age groups in slow RT trials with a neutral prime as a result of an endogenous early intention to respond in a direction opposite the eventual instructing arrow cue. We conclude that the basic behavioral and electrophysiological signatures of implicit ChoI are common to a wide range of ages. However, older subjects, despite showing a similar dynamic decision trajectory as younger adults, are slower, more prudent and finalize the decision making process before letting the information affect the peripheral motor system. In contrast, the flow of information in younger subjects occurs in parallel to the decision process.

Preserved left and upper visual field advantages in older adults' orienting of attention.

Lateralization of the distribution of attentional function in the brain is asserted to lead to asymmetry in attentional allocation. This is expressed in the phenomenon of pseudoneglect, in which line and object bisection judgments indicate left visual field (and presumably right hemisphere) dominance. Several studies indicate that this asymmetry is not found in old age, which is taken as an indication of decline in attentional function with aging. We examined this assertion using a more comprehensive assay of attentional asymmetry. We contrasted the spatial distribution of older and younger adults' visual attention using the Starry Night Task, a speeded visual search task in which targets must be located across a wide spatial distribution against a dynamic background of distracters. As expected, compared to younger adults, older adults' response times were longer overall. However, we found that older adults exhibited a graded left visual field advantage, even more distinctly than did younger adults. Additionally, older adults exhibited a graded upper visual field advantage equivalent to that of younger adults. These results indicate that aging may not necessarily compromise basic patterns of distribution of spatial attention. They do not support claims of aging-related loss of attentional lateralization.

Evidence for Linear but Not Helical Automatic Representation of Pitch in the Human Auditory System.

The perceptual organization of pitch is frequently described as helical, with a monotonic dimension of pitch height and a circular dimension of pitch chroma, accounting for the repeating structure of the octave. Although the neural representation of pitch height is widely studied, the way in which pitch chroma representation is manifested in neural activity is currently debated. We tested the automaticity of pitch chroma processing using the MMN-an ERP component indexing automatic detection of deviations from auditory regularity. Musicians trained to classify pure or complex tones across four octaves, based on chroma-C versus G (21 participants, Experiment 1) or C versus F# (27, Experiment 2). Next, they were passively exposed to MMN protocols designed to test automatic detection of height and chroma deviations. Finally, in an "attend chroma" block, participants had to detect the chroma deviants in a sequence similar to the passive MMN sequence. The chroma deviant tones were accurately detected in the training and the attend chroma parts both for pure and complex tones, with a slightly better performance for complex tones. However, in the passive blocks, a significant MMN was found only to height deviations and complex tone chroma deviations, but not to pure tone chroma deviations, even for perfect performers in the active tasks. These results indicate that, although height is represented preattentively, chroma is not. Processing the musical dimension of chroma may require higher cognitive processes, such as attention and working memory.

Systematic comparison between a wireless EEG system with dry electrodes and a wired EEG system with wet electrodes.

Recent advances in dry electrodes technology have facilitated the recording of EEG in situations not previously possible, thanks to the relatively swift electrode preparation and avoidance of applying gel to subject's hair. However, to become a true alternative, these systems should be compared to state-of-the-art wet EEG systems commonly used in clinical or research applications. In our study, we conducted a systematic comparison of electrodes application speed, subject comfort, and most critically electrophysiological signal quality between the conventional and wired Biosemi EEG system using wet active electrodes and the compact and wireless F1 EEG system consisting of dry passive electrodes. All subjects (n = 27) participated in two recording sessions on separate days, one with the wet EEG system and one with the dry EEG system, in which the session order was counterbalanced across subjects. In each session, we recorded their EEG during separate rest periods with eyes open and closed followed by two versions of a serial visual presentation target detection task. Each task component allows for a neural measure reflecting different characteristics of the data, including spectral power in canonical low frequency bands, event-related potential components (specifically, the P3b), and single trial classification based on machine learning. The performance across the two systems was similar in most measures, including the P3b amplitude and topography, as well as low frequency (theta, alpha, and beta) spectral power at rest. Both EEG systems performed well above chance in the classification analysis, with a marginal advantage of the wet system over the dry. Critically, all aforementioned electrophysiological metrics showed significant positive correlations (r = 0.54-0.89) between the two EEG systems. This multitude of measures provides a comprehensive comparison that captures different aspects of EEG data, including temporal precision, frequency domain as well as multivariate patterns of activity. Taken together, our results indicate that the dry EEG system used in this experiment can effectively record electrophysiological measures commonly used across the research and clinical contexts with comparable quality to the conventional wet EEG system.

Direct Evidence for Prediction Signals in Frontal Cortex Independent of Prediction Error.

Predictive coding (PC) has been suggested as one of the main mechanisms used by brains to interact with complex environments. PC theories posit top-down prediction signals, which are compared with actual outcomes, yielding in turn prediction error (PE) signals, which are used, bottom-up, to modify the ensuing predictions. However, disentangling prediction from PE signals has been challenging. Critically, while many studies found indirect evidence for PC in the form of PE signals, direct evidence for the prediction signal is mostly lacking. Here, we provide clear evidence, obtained from intracranial cortical recordings in human surgical patients, that the human lateral prefrontal cortex evinces prediction signals while anticipating an event. Patients listened to task-irrelevant sequences of repetitive tones including infrequent predictable or unpredictable pitch deviants. The broadband high-frequency amplitude (HFA) was decreased prior to the onset of expected relative to unexpected deviants in the frontal cortex only, and its amplitude was sensitive to the increasing likelihood of deviants following longer trains of standards in the unpredictable condition. Single-trial HFA predicted deviations and correlated with poststimulus response to deviations. These results provide direct evidence for frontal cortex prediction signals independent of PE signals.

Human posterior parietal cortex responds to visual stimuli as early as peristriate occipital cortex.

Much of what is known about the timing of visual processing in the brain is inferred from intracranial studies in monkeys, with human data limited to mainly noninvasive methods with lower spatial resolution. Here, we estimated visual onset latencies from electrocorticographic (ECoG) recordings in a patient who was implanted with 112 subdural electrodes, distributed across the posterior cortex of the right hemisphere, for presurgical evaluation of intractable epilepsy. Functional MRI prior to surgery was used to determine boundaries of visual areas. The patient was presented with images of objects from several categories. Event-related potentials (ERPs) were calculated across all categories excluding targets, and statistically reliable onset latencies were determined, using a bootstrapping procedure over the single trial baseline activity in individual electrodes. The distribution of onset latencies broadly reflected the known hierarchy of visual areas, with the earliest cortical responses in primary visual cortex, and higher areas showing later responses. A clear exception to this pattern was a robust, statistically reliable and spatially localized, very early response, on the bank of the posterior intraparietal sulcus (IPS). The response in the IPS started nearly simultaneously with responses detected in peristriate visual areas, around 60 ms poststimulus onset. Our results support the notion of early visual processing in the posterior parietal lobe, not respecting traditional hierarchies, and give direct evidence for onset times of visual responses across the human cortex.

Alternative outcomes create biased expectations regarding the received outcome: Evidence from event-related potentials.

After choosing between uncertain options, one might get feedback on both the outcome of the chosen option and the outcome of the unchosen option (the alternative). Behavioral research has shown that in such cases people engage in outcome comparison, and that the alternative outcome influences the way one evaluates his own received outcome. Moreover, this influence differs whether one was responsible or not for the choice made. In two studies, we looked for the electrophysiological correlates of outcome comparison. Subjects chose one of two boxes shown on the screen, each box contained a gain or a loss. The alternative outcome was always revealed first, followed by the received outcome. In half of the trials the software picked one box instead of subjects. We tested whether the feedback-related negativity (FRN) and the P3 elicited by the received reflect outcome comparison. As expected, we found that the FRN and P3 were more positive when the received outcome was a gain (vs. a loss). The FRN and P3 were also sensitive to the value of the alternative outcome, but contrary to our predictions, they were more positive when the alternative outcome was a gain (vs. a loss). As the FRN and P3 are sensitive to expectations, we hypothesized that our findings might result from subjects' biased expectations: subjects might have wrongly believed that a good (bad) alternative outcome signaled a bad (good) received outcome. This hypothesis, coined as the Alternative Omen Effect, was confirmed in parallel in a series of behavioral experiments: people see an illusory negative correlation between the uncorrelated outcomes of choice options (reported in Marciano-Romm et al. (2016)). A challenge for future research will be to disentangle the effects of expectation from those of outcome comparison.

Increasing suppression of saccade-related transients along the human visual hierarchy.

A key hallmark of visual perceptual awareness is robustness to instabilities arising from unnoticeable eye and eyelid movements. In previous human intracranial (iEEG) work (Golan et al., 2016) we found that excitatory broadband high-frequency activity transients, driven by eye blinks, are suppressed in higher-level but not early visual cortex. Here, we utilized the broad anatomical coverage of iEEG recordings in 12 eye-tracked neurosurgical patients to test whether a similar stabilizing mechanism operates following small saccades. We compared saccades (1.3°-3.7°) initiated during inspection of large individual visual objects with similarly-sized external stimulus displacements. Early visual cortex sites responded with positive transients to both conditions. In contrast, in both dorsal and ventral higher-level sites the response to saccades (but not to external displacements) was suppressed. These findings indicate that early visual cortex is highly unstable compared to higher-level visual regions which apparently constitute the main target of stabilizing extra-retinal oculomotor influences.

Cortical representation of persistent visual stimuli.

Research into visual neural activity has focused almost exclusively on onset- or change-driven responses and little is known about how information is encoded in the brain during sustained periods of visual perception. We used intracranial recordings in humans to determine the degree to which the presence of a visual stimulus is persistently encoded by neural activity. The correspondence between stimulus duration and neural response duration was strongest in early visual cortex and gradually diminished along the visual hierarchy, such that is was weakest in inferior-temporal category-selective regions. A similar posterior-anterior gradient was found within inferior temporal face-selective regions, with posterior but not anterior sites showing persistent face-selective activity. The results suggest that regions that appear uniform in terms of their category selectivity are dissociated by how they temporally represent a stimulus in support of ongoing visual perception, and delineate a large-scale organizing principle of the ventral visual stream.