Pre-stimulus Neural Activity Research Articles

Pre-stimulus neural activity and visual perception in schizophrenia

Pre-stimulus neural activity and visual perception in schizophrenia

Initial conditions combine with sensory evidence to induce decision-related dynamics in premotor cortex

We used a dynamical systems perspective to understand decision-related neural activity, a fundamentally unresolved problem. This perspective posits that time-varying neural activity is described by a state equation with an initial condition and evolves in time by combining at each time step, recurrent activity and inputs. We hypothesized various dynamical mechanisms of decisions, simulated them in models to derive predictions, and evaluated these predictions by examining firing rates of neurons in the dorsal premotor cortex (PMd) of monkeys performing a perceptual decision-making task. Prestimulus neural activity (i.e., the initial condition) predicted poststimulus neural trajectories, covaried with RT and the outcome of the previous trial, but not with choice. Poststimulus dynamics depended on both the sensory evidence and initial condition, with easier stimuli and fast initial conditions leading to the fastest choice-related dynamics. Together, these results suggest that initial conditions combine with sensory evidence to induce decision-related dynamics in PMd.

Task demands modulate pre-stimulus alpha frequency and sensory template during bistable apparent motion perception.

Despite ambiguous environmental inputs, top-down attention biases our subjective perception toward the preferred percepts, via modulating prestimulus neural activity or inducing prestimulus sensory templates that carry concrete internal sensory representations of the preferred percepts. In contrast to frequent changes of behavioral goals in the typical cue-target paradigm, human beings are often engaged in a prolonged task state with only 1 specific behavioral goal. It remains unclear how prestimulus neural signals and sensory templates are modulated in the latter case. To answer this question in the present electroencephalogram study on human subjects, we manipulated sustained task demands toward one of the 2 possible percepts in the bistable Ternus display, emphasizing either temporal integration or segregation. First, the prestimulus peak alpha frequency, which gated the temporal window of temporal integration, was effectively modulated by task demands. Furthermore, time-resolved decoding analyses showed that task demands biased neural representations toward the preferred percepts after the full presentation of bottom-up stimuli. More importantly, sensory templates resembling the preferred percepts emerged even before the bottom-up sensory evidence were sufficient enough to induce explicit percepts. Taken together, task demands modulate both prestimulus alpha frequency and sensory templates, to eventually bias subjective perception toward the preferred percepts.

Monitoring Brain State and Behavioral Performance during Repetitive Visual Stimulation

We tested whether changes in prestimulus neural activity predict behavioral performance (decision time and errors) during a prolonged visual task. The task was to classify ambiguous stimuli—Necker cubes; manipulating the degree of ambiguity from low ambiguity (LA) to high ambiguity (HA) changed the task difficulty. First, we assumed that the observer’s state changes over time, which leads to a change in the prestimulus brain activity. Second, we supposed that the prestimulus state produces a different effect on behavioral performance depending on the task demands. Monitoring behavioral responses, we revealed that the observer’s decision time decreased for both LA and HA stimuli during the task performance. The number of perceptual errors lowered for HA, but not for LA stimuli. EEG analysis revealed an increase in the prestimulus 9–11 Hz EEG power with task time. Finally, we found associations between the behavioral and neural estimates. The prestimulus EEG power negatively correlated with the decision time for LA stimuli and the erroneous responses rate for HA stimuli. The obtained results confirm that monitoring prestimulus EEG power enables predicting perceptual performance on the behavioral level. The observed different time-on-task effects on the LA and HA stimuli processing may shed light on the features of ambiguous perception.

Cannabis use impacts pre-stimulus neural activity in the visual cortices of people with HIV.

People with HIV (PWH) use cannabis at a higher rate than the general population, but the influence on neural activity is not well characterized. Cannabis use among PWH may have a beneficial effect, as neuroinflammation is known to be a critical problem in PWH and cannabis use has been associated with a reduction in proinflammatory markers. Thus, it is important to understand the net impact of cannabis use on brain and cognitive function in PWH. In this study, we collected magnetoencephalographic (MEG) brain imaging data on 81 participants split across four demographically matched groups (i.e., PWH using cannabis, controls using cannabis, non‐using PWH, and non‐using controls). Participants completed a visuospatial processing task during MEG. Time–frequency resolved voxel time series were extracted to identify the dynamics of oscillatory and pre‐stimulus baseline neural activity. Our results indicated strong theta (4–8 Hz), alpha (10–16 Hz), and gamma (62–72 Hz) visual oscillations in parietal–occipital brain regions across all participants. PWH exhibited significant behavioral deficits in visuospatial processing, as well as reduced theta oscillations and elevated pre‐stimulus gamma activity in visual cortices, all of which replicate prior work. Strikingly, chronic cannabis use was associated with a significant reduction in pre‐stimulus gamma activity in the visual cortices, such that PWH no longer statistically differed from controls. These results provide initial evidence that cannabis use may normalize some neural aberrations in PWH. This study fills an important gap in understanding the impact of cannabis use on brain and cognitive function in PWH.

Text type attribution modulates pre-stimulus alpha power in sentence reading

Prior knowledge and context-specific expectations influence the perception of sensory events, e.g., speech, as well as complex higher-order cognitive operations like text reading. Here, we focused on pre-stimulus neural activity during sentence reading to examine text type-dependent attentional bias in anticipation of written stimuli, capitalizing on the functional relevance of brain oscillations in the alpha (8–12 Hz) frequency range. Two sex- and age-matched groups of participants (n = 24 each) read identical sentences on a screen at a fixed per-constituent presentation rate while their electroencephalogram was recorded; the groups were differentially instructed to read “sentences” (genre-neutral condition) or “verses from poems” (poetry condition). Relative alpha power (pre-cue vs. post-cue) in pre-stimulus time windows was greater in the poetry condition than in the genre-neutral condition. This finding constitutes initial evidence for genre-specific cognitive adjustments that precede processing proper, and potentially links current theories of discourse comprehension to current theories of brain function.

Effects of Age on Prestimulus Neural Activity Predictive of Successful Memory Encoding: An fMRI Study.

Prestimulus subsequent memory effects (SMEs)-differences in neural activity preceding the onset of study items that are predictive of later memory performance-have consistently been reported in young adults. The present functional magnetic resonance imaging experiment investigated potential age-related differences in prestimulus SMEs. During study, healthy young and older participants made one of two semantic judgments on images, with the judgment signaled by a preceding cue. In test phase, participants first made an item recognition judgment and, for each item judged old, a source memory judgment. Age-invariant prestimulus SMEs were observed in left dorsomedial prefrontal cortex, left hippocampus, and right subgenual cortex. In each case, the effects reflected lower blood oxygen level dependent signal for later recognized items, regardless of source accuracy, than for unrecognized items. A similar age-invariant pattern was observed in left orbitofrontal cortex, but this effect was specific to items attracting a correct source response compared to unrecognized items. In contrast, the left angular gyrus and fusiform cortex demonstrated negative prestimulus SMEs that were exclusive to young participants. The findings indicate that age differences in prestimulus SMEs are regionally specific and suggest that prestimulus SMEs reflect multiple cognitive processes, only some of which are vulnerable to advancing age.

Momentary lapses of attention in multisensory environment

Momentary lapses in attention disrupt goal-directed behaviors, and have been associated with increased pre-stimulus activity in the default mode network (DMN). The human brain often encounters multisensory inputs. It remains unknown, however, whether the neural mechanisms underlying attentional lapses are supra-modal or modality-dependent. To answer this question in the present functional magnetic resonance imaging (fMRI) study, we asked participants to respond to either visual or auditory targets in a multisensory paradigm, and focused on the pre-stimulus neural signals underlying attentional lapses, which resulted in impaired task performance, in terms of both delayed RTs and behavioral errors, in different sensory modalities. Behaviorally, mean reaction times (RTs) were equivalent between the visual and auditory modality. At the neural level, increased pre-stimulus neural activity in the majority of the core DMN regions, including medial prefrontal cortex (mPFC), posterior cingulate cortex (PCC), and left angular gyrus (AG), predicted delayed RTs more effectively in the visual than auditory modality. Especially, increased pre-stimulus activity in the mPFC predicted not only delayed RTs but also errors, more effectively in the visual than auditory modality. On the other hand, increased pre-stimulus activity in the anterior precuneus predicted both prolonged RTs and errors more effectively in the auditory than visual modality. Moreover, a supra-modal mechanism was revealed in the left middle temporal gyrus (MTG), which belongs to the posterior DMN. Increased pre-stimulus neural activity in the left MTG predicted impaired task performance in both the visual and auditory modality. Taken together, the core DMN regions manifest vision-dependent mechanisms of attentional lapses while a novel region in the anterior precuneus shows audition-dependent mechanisms of attentional lapses. Moreover, left MTG in the posterior DMN manifests a supra-modal mechanism of attentional lapses, independent of the modality of sensory inputs.

Converging intracortical signatures of two separated processing timescales in human early auditory cortex

Neural oscillations in auditory cortex are argued to support parsing and representing speech constituents at their corresponding temporal scales. Yet, how incoming sensory information interacts with ongoing spontaneous brain activity, what features of the neuronal microcircuitry underlie spontaneous and stimulus-evoked spectral fingerprints, and what these fingerprints entail for stimulus encoding, remain largely open questions. We used a combination of human invasive electrophysiology, computational modeling and decoding techniques to assess the information encoding properties of brain activity and to relate them to a plausible underlying neuronal microarchitecture. We analyzed intracortical auditory EEG activity from 10 patients while they were listening to short sentences. Pre-stimulus neural activity in early auditory cortical regions often exhibited power spectra with a shoulder in the delta range and a small bump in the beta range. Speech decreased power in the beta range, and increased power in the delta-theta and gamma ranges. Using multivariate machine learning techniques, we assessed the spectral profile of information content for two aspects of speech processing: detection and discrimination. We obtained better phase than power information decoding, and a bimodal spectral profile of information content with better decoding at low (delta-theta) and high (gamma) frequencies than at intermediate (beta) frequencies. These experimental data were reproduced by a simple rate model made of two subnetworks with different timescales, each composed of coupled excitatory and inhibitory units, and connected via a negative feedback loop. Modeling and experimental results were similar in terms of pre-stimulus spectral profile (except for the iEEG beta bump), spectral modulations with speech, and spectral profile of information content. Altogether, we provide converging evidence from both univariate spectral analysis and decoding approaches for a dual timescale processing infrastructure in human auditory cortex, and show that it is consistent with the dynamics of a simple rate model.

Exploring the role of expectations and stimulus relevance on stimulus-specific neural representations and conscious report.

Subjective experience can be influenced by top-down factors, such as expectations and stimulus relevance. Recently, it has been shown that expectations can enhance the likelihood that a stimulus is consciously reported, but the neural mechanisms supporting this enhancement are still unclear. We manipulated stimulus expectations within the attentional blink (AB) paradigm using letters and combined visual psychophysics with magnetoencephalographic (MEG) recordings to investigate whether prior expectations may enhance conscious access by sharpening stimulus-specific neural representations. We further explored how stimulus-specific neural activity patterns are affected by the factors expectation, stimulus relevance and conscious report. First, we show that valid expectations about the identity of an upcoming stimulus increase the likelihood that it is consciously reported. Second, using a series of multivariate decoding analyses, we show that the identity of letters presented in and out of the AB can be reliably decoded from MEG data. Third, we show that early sensory stimulus-specific neural representations are similar for reported and missed target letters in the AB task (active report required) and an oddball task in which the letter was clearly presented but its identity was task-irrelevant. However, later sustained and stable stimulus-specific representations were uniquely observed when target letters were consciously reported (decision-dependent signal). Fourth, we show that global pre-stimulus neural activity biased perceptual decisions for a ‘seen’ response. Fifth and last, no evidence was obtained for the sharpening of sensory representations by top-down expectations. We discuss these findings in light of emerging models of perception and conscious report highlighting the role of expectations and stimulus relevance.

Pre-stimulus theta power is correlated with variation of motor evoked potential latency: a single-pulse TMS study

There has been a growing interest in the role of pre-stimulus oscillations on cortical excitability in visual and motor systems. Prior studies focused on the relationship between pre-stimulus neuronal activity and TMS-evoked motor evoked potentials (MEPs) have reported heterogeneous results. We aimed to assess the role of pre-stimulus neural activity on the latency of MEPs, which might enhance our understanding of the variability of MEP signals, and potentially provide information on the role played by cortical activity fluctuations in the excitability of corticospinal pathways. Near-threshold single-pulse TMS (spTMS) was applied at random intervals over the primary motor cortex of 14 healthy participants while they sat passively, to trigger hand muscle contractions. Multichannel EEG was recorded during spTMS blocks. Spearman correlations between both the variation in MEP onset latencies and peak-to-peak MEP amplitudes, and the pre-stimulus power of EEG oscillations were calculated across participants. We found that the variation in MEP latency was positively correlated with pre-stimulus power in the theta range (4-7Hz) in a broad time window (- 3.1 to - 1.9s) preceding the spTMS generating the MEP. No correlation between pre-stimulus power in any frequency band and MEP amplitude was found. Our results show that pre-stimulus theta oscillations are correlated with the variation in MEP latency, an outcome measure determined by fiber conduction velocity and synaptic delays along the corticospinal tract. This finding could prove useful for clinicians using MEP latency-based information in pre- or intra-operative diagnostics of corticospinal impairment.

Variations in prestimulus neural activity predict the emotion-enhanced memory effect.

Here, we report evidence that electrophysiological neural activity preceding the onset of emotional pictures can predict whether they will be remembered or forgotten 24 h later, whereas the same effect was not observed for neutral pictures. In contrast to previous research, we observed this effect using a paradigm in which participants could not predict the emotional or the neutral content of the pictures before their onset. These effects were obtained alongside significant behavioural effects of superior recognition memory for emotional compared with neutral items. These findings suggest that the preferential encoding of emotional events in memory is determined by fluctuations in the availability of processing resources just before event onset. This explanation argues in favour of mediational models of emotional memory, which contend that emotional information is preferentially encoded because it mobilizes a greater amount of processing resources than neutral information.

The Role of Working Memory in the Probabilistic Inference of Future Sensory Events.

The ability to represent the emerging regularity of sensory information from the external environment has been thought to allow one to probabilistically infer future sensory occurrences and thus optimize behavior. However, the underlying neural implementation of this process is still not comprehensively understood. Through a convergence of behavioral and neurophysiological evidence, we establish that the probabilistic inference of future events is critically linked to people's ability to maintain the recent past in working memory. Magnetoencephalography recordings demonstrated that when visual stimuli occurring over an extended time series had a greater statistical regularity, individuals with higher working-memory capacity (WMC) displayed enhanced slow-wave neural oscillations in the θ frequency band (4-8 Hz.) prior to, but not during stimulus appearance. This prestimulus neural activity was specifically linked to contexts where information could be anticipated and influenced the preferential sensory processing for this visual information after its appearance. A separate behavioral study demonstrated that this process intrinsically emerges during continuous perception and underpins a realistic advantage for efficient behavioral responses. In this way, WMC optimizes the anticipation of higher level semantic concepts expected to occur in the near future.

Shaping prestimulus neural activity with auditory rhythmic stimulation improves the temporal allocation of attention.

Human attention fluctuates across time, and even when stimuli have identical physical characteristics and the task demands are the same, relevant information is sometimes consciously perceived and at other times not. A typical example of this phenomenon is the attentional blink, where participants show a robust deficit in reporting the second of two targets (T2) in a rapid serial visual presentation (RSVP) stream. Previous electroencephalographical (EEG) studies showed that neural correlates of correct T2 report are not limited to the RSVP period, but extend before visual stimulation begins. In particular, reduced oscillatory neural activity in the alpha band (8-12 Hz) before the onset of the RSVP has been linked to lower T2 accuracy. We therefore examined whether auditory rhythmic stimuli presented at a rate of 10 Hz (within the alpha band) could increase oscillatory alpha-band activity and improve T2 performance in the attentional blink time window. Behaviourally, the auditory rhythmic stimulation worked to enhance T2 accuracy. This enhanced perception was associated with increases in the posterior T2-evoked N2 component of the event-related potentials and this effect was observed selectively at lag 3. Frontal and posterior oscillatory alpha-band activity was also enhanced during auditory stimulation in the pre-RSVP period and positively correlated with T2 accuracy. These findings suggest that ongoing fluctuations can be shaped by sensorial events to improve the allocation of attention in time.

The contribution of pre-stimulus neural oscillatory activity to spontaneous response time variability

Large variability between individual response times, even in identical conditions, is a ubiquitous property of animal behavior. However, the origins of this stochasticity and its relation to action decisions remain unclear. Here we focus on the state of the perception–action network in the pre-stimulus period and its influence on subsequent saccadic response time and choice in humans. We employ magnetoencephalography (MEG) and a correlational source reconstruction approach to identify the brain areas where pre-stimulus oscillatory activity predicted saccadic response time to visual targets. We find a relationship between future response time and pre-stimulus power, but not phase, in occipital (including V1), parietal, posterior cingulate and superior frontal cortices, consistently across alpha, beta and low gamma frequencies, each accounting for between 1 and 4% of the RT variance. Importantly, these correlations were not explained by deterministic sources of variance, such as experimental factors and trial history. Our results further suggest that occipital areas mainly reflect short-term (trial to trial) stochastic fluctuations, while the frontal contribution largely reflects longer-term effects such as fatigue or practice. Parietal areas reflect fluctuations at both time scales. We found no evidence of lateralization: these effects were indistinguishable in both hemispheres and for both saccade directions, and non-predictive of choice — a finding with fundamental consequences for models of action decision, where independent, not coupled, noise is normally assumed.

Pre-stimulus neural activity predicts successful encoding of inter-item associations

fMRI was employed to investigate the relationship between pre-stimulus neural activity and associative encoding of words and pictures in humans. While undergoing scanning, subjects studied randomly interleaved word or picture pairs. A pre-stimulus cue preceded the presentation of each study pair and signaled whether it would comprise words or pictures. Memory for the study pairs was later tested with an associative recognition test, which comprised word or picture pairs presented either in the same (intact) or a different (rearranged) pairing as at study, along with pairs of new items. The critical fMRI contrast was between study activity associated with pairs later correctly judged intact and pairs incorrectly judged as rearranged. A key question was whether material-selective pre-stimulus encoding effects could be identified which overlapped regions selectively activated by the respective study material. Picture-selective pre-stimulus effects were identified in bilateral fusiform and the intraparietal sulcus (IPS), whereas word-selective effects could not be identified. Material-invariant pre-stimulus subsequent memory effects were also identified in several neocortical regions as well as in the hippocampus. Whereas the loci of the neocortical effects suggest that they reflect the benefit to encoding that accrues from engagement of cognitive control processes, their magnitude was negatively correlated across subjects with associative recognition performance and positively related to false alarm rate. Conversely, the hippocampal effects also predicted unique variance in associative memory and were negatively related to hit rate. It is suggested that the neocortical pre-stimulus effects may reflect encoding processes that increase familiarity of single items, whereas the hippocampal pre-stimulus effects are proposed to reflect either the encoding of task-irrelevant features or the retrieval of task-relevant information associated with the pre-stimulus cues. Overall, the results provide evidence that pre-stimulus processes may be deleterious, rather than beneficial, to associative encoding.

Conscious Access Is Linked to Ongoing Brain State: Electrophysiological Evidence from the Attentional Blink

Neuroscience explanations of conscious access focus on neural events elicited by stimuli. In contrast, here, we used the attentional blink paradigm in combination with event-related brain potentials to examine whether the ongoing state of the brain before a stimulus can determine both conscious access and the poststimulus neural events associated with consciousness. Participants were required to detect 2 target letters from digit distractors while their brain activity was being recorded. Trials were classified based on whether the secondcritical target (T2) was detected. We found that T2-detection was predetermined by brain activity prior to the onset of the stimulation stream. Specifically, T2-detected trials were predicated by a frontocentral positive going deflection that started more than 200 ms before the stream began. Accurate T2 detection was also accompanied by enhanced poststimulus neural activity, as reflected by a larger P3b component. Furthermore, prestimulus and poststimulus markers of T2-detection were highly correlated with one another. We therefore argue that conscious experiences are shaped by potentially random fluctuations in neural activity. Overall, the results reveal that conscious access is underpinned by an important relationship involving predictive prestimulus neural activity and responsive poststimulus brain activity.

From Prestimulus Alpha Oscillation to Visual-evoked Response: An Inverted-U Function and Its Attentional Modulation

Understanding the relation between prestimulus neural activity and subsequent stimulus processing has become an area of active investigation. Computational modeling, as well as in vitro and in vivo single-unit recordings in animal preparations, have explored mechanisms by which background synaptic activity can influence the responsiveness of cortical neurons to afferent input. How these mechanisms manifest in humans is not well understood. Although numerous EEG/MEG studies have considered the role of prestimulus alpha oscillations in the genesis of visual-evoked potentials, no consensus has emerged, and divergent reports continue to appear. The present work addresses this problem in three stages. First, a theoretical model was developed in which the background synaptic activity and the firing rate of a neural ensemble are related through a sigmoidal function. The derivative of this function, referred to as local gain, has an inverted-U shape and is postulated to be proportional to the trial-by-trial response evoked by a transient stimulus. Second, the theoretical model was extended to noninvasive studies of human visual processing, where the model variables are reinterpreted in terms of ongoing EEG oscillations and event-related potentials. Predictions were derived from the model and tested by recording high-density scalp EEG from healthy volunteers performing a trial-by-trial cued spatial visual attention task. Finally, enhanced stimulus processing by attention was linked to an increase in the overall slope of the sigmoidal function. The commonly observed reduction of alpha magnitude with attention was interpreted as signaling a shift of the underlying neural ensemble toward an optimal excitability state that enables the increase in global gain.

Medial Temporal Theta/Alpha Power Enhancement Precedes Successful Memory Encoding: Evidence Based on Intracranial EEG

Not only poststimulus, but also prestimulus neural activity has been shown to be predictive for later successful memory encoding. However, it is still not clear which medial temporal lobe processes precede effective memory formation. Here, our aim was to investigate whether such prestimulus markers for successful memory encoding can be specified based on intracranial recordings directly from the hippocampus and rhinal cortex. For this purpose, we analyzed subsequent memory effects during a continuous word recognition paradigm in 31 presurgical epilepsy patients. We found that rhinal and hippocampal theta and successive alpha power enhancement before word presentation predicted successful memory encoding. Previous studies suggest that stimulus-triggered hippocampal theta activity is particularly related to memory retrieval and activation of a mnemonic context, whereas the alpha rhythm reflects inhibitory top-down control of task processing and executive functioning. In line with these suggestions, we propose that the observed medial temporal theta and alpha power increases before stimulus presentation reflect activation of contextual information and inhibitory top-down control processes preparing for stimulus-triggered memory processing.

The influence of aging and frontal function on the neural correlates of regulative and evaluative aspects of cognitive control.

The influence of aging and frontal function on the neural correlates of regulative and evaluative control was examined by means of event-related brain potentials (ERPs). The behavioral data indicated that interference was greater for older than for younger adults and that this difference was mediated by frontal function. The ERP data revealed effects of aging on the neural correlates of both regulative and evaluative control. Prestimulus neural activity was correlated with response time and frontal function, and these relationships were moderated by the response-to-stimulus interval (RSI); the poststimulus data also revealed age-related differences in the neural correlates of evaluative control that interacted with RSI. These data support predictions derived from the context processing deficit theory of aging.