Pre-stimulus influences on auditory perception arising from sensory representations and decision processes

The qualities of perception depend not only on the sensory inputs but also on the brain state before stimulus presentation. Although the collective evidence from neuroimaging studies for a relation between prestimulus state and perception is strong, the interpretation in the context of sensory computations or decision processes has remained difficult. In the auditory system, for example, previous studies have reported a wide range of effects in terms of the perceptually relevant frequency bands and state parameters (phase/power). To dissociate influences of state on earlier sensory representations and higher-level decision processes, we collected behavioral and EEG data in human participants performing two auditory discrimination tasks relying on distinct acoustic features. Using single-trial decoding, we quantified the relation between prestimulus activity, relevant sensory evidence, and choice in different task-relevant EEG components. Within auditory networks, we found that phase had no direct influence on choice, whereas power in task-specific frequency bands affected the encoding of sensory evidence. Within later-activated frontoparietal regions, theta and alpha phase had a direct influence on choice, without involving sensory evidence. These results delineate two consistent mechanisms by which prestimulus activity shapes perception. However, the timescales of the relevant neural activity depend on the specific brain regions engaged by the respective task

Ongoing neural oscillations influence behavior and sensory representations by suppressing neuronal excitability

The ability to process and respond to external input is critical for adaptive behavior. Why, then, do neural and behavioral responses vary across repeated presentations of the same sensory input? Ongoing fluctuations of neuronal excitability are currently hypothesized to underlie the trial-by-trial variability in sensory processing. To test this, we capitalized on intracranial electrophysiology in neurosurgical patients performing an auditory discrimination task with visual cues: specifically, we examined the interaction between prestimulus alpha oscillations, excitability, task performance, and decoded neural stimulus representations. We found that strong prestimulus oscillations in the alpha+ band (i.e., alpha and neighboring frequencies), rather than the aperiodic signal, correlated with a low excitability state, indexed by reduced broadband high-frequency activity. This state was related to slower reaction times and reduced neural stimulus encoding strength. We propose that the alpha+ rhythm modulates excitability, thereby resulting in variability in behavior and sensory representations despite identical input

Prestimulus influences on auditory perception from sensory representations and decision processes

Kayser S, McNair SW, Kayser C. Prestimulus influences on auditory perception from sensory representations and decision processes. Proc Natl Acad Sci U S A. 2016;113(17):4842-7

Cortical alpha activity predicts the confidence in an impending action

When we make a decision, we experience a degree of confidence that our choice may lead to a desirable outcome. Recent studies in animals have probed the subjective aspects of the choice confidence using confidence-reporting tasks. These studies showed that estimates of the choice confidence substantially modulate neural activity in multiple regions of the brain. Building on these findings, we investigated the neural representation of the confidence in a choice in humans who explicitly reported the confidence in their choice. Subjects performed a perceptual decision task in which they decided between choosing a button press or a saccade while we recorded EEG activity. Following each choice, subjects indicated whether they were sure or unsure about the choice. We found that alpha activity strongly encodes a subject's confidence level in a forthcoming button press choice. The neural effect of the subjects' confidence was independent of the reaction time and independent of the sensory input modeled as a decision variable. Furthermore, the effect is not due to a general cognitive state, such as reward expectation, because the effect was specifically observed during button press choices and not during saccade choices. The neural effect of the confidence in the ensuing button press choice was strong enough that we could predict, from independent single trial neural signals, whether a subject was going to be sure or unsure of an ensuing button press choice. In sum, alpha activity in human cortex provides a window into the commitment to make a hand movement

Pre-stimulus alpha activity modulates face and object processing in the intra-parietal sulcus, a MEG study

Face perception is crucial in all social animals. Recent studies have shown that pre-stimulus oscillations of brain activity modulate the perceptual performance of face vs. non-face stimuli, specifically under challenging conditions. However, it is unclear if this effect also occurs during simple tasks, and if so in which brain regions. Here we used magnetoencephalography (MEG) and a 1-back task in which participants decided if the two sequentially presented stimuli were the same or not in each trial. The aim of the study was to explore the effect of pre-stimulus alpha oscillation on the perception of face (human and monkey) and non-face stimuli. Our results showed that pre-stimulus activity in the left occipital face area (OFA) modulated responses in the intra-parietal sulcus (IPS) at around 170 ms after the presentation of human face stimuli. This effect was also found after participants were shown images of motorcycles. In this case, the IPS was modulated by pre-stimulus activity in the right OFA and the right fusiform face area (FFA). We conclude that pre-stimulus modulation of post-stimulus response also occurs during simple tasks and is therefore independent of behavioral responses

Divide and conquer: an oscillatory division of labour in service of episodic memory

Both oscillatory synchronisation and oscillatory desynchronisation underpin the formation and retrieval of episodic memories. This paradox begs the question: how can two polar opposite neural phenomena produce the same outcome? Here, we investigate this conundrum by presenting a series of empirical experiments that test the hypothesis that these two phenomena reflect a division of labour in service of episodic memory. We demonstrate that neocortical desynchrony correlates with enhanced information representation, while hippocampal synchrony stiches this information together into a coherent memory trace. Critically, we demonstrate that these processes interact. Neocortical desynchrony precedes and predicts hippocampal synchrony during episodic memory formation, while hippocampal synchrony precedes and predicts neocortical desynchrony during episodic memory retrieval. This thesis suggests that the interaction between neocortical desynchrony and hippocampal synchrony sits at the heart of the formation and retrieval of episodic memories, providing empirical resolution to the so-called synchronisation/desynchronisation conundrum

Context-oriented performance biases in cognitive control

Cognitive control, the ability to guide goal-directed behavior, is comprised of a variety of cognitive components functioning in a dynamic balance. Control adjustments are commonly cast as temporally local adaptations reflecting recently encountered task conflict; however, global control processes representing broad task expectancies are relatively unexplored. In an electroencephalographic (EEG) study of a prepotent response inhibition task, we tested whether the congruency effect, where performance tends to be worse for trials involving controlled processes, would be impacted by the overall task context as defined by trial-type proportions. As the proportion of high-control trials increased, we observed that accuracy improved in a more demanding, high-control condition while worsening in the less demanding, low-control condition. More interestingly, this tradeoff resulted in a reversed congruency effect in accuracy for task contexts dominated by high control trials. Furthermore, delay period EEG spectral power in the alpha-frequency band (i.e., 9-13 Hz)—a putative inhibitory mechanism (Klimesch, 2012)—was found to modulate with the task. A significant trial condition by task context interaction revealed a positive monotonic association between accuracy and induced alpha synchrony in low control task contexts with a negative monotonic association in the high control context. Our behavioral results are consistent with cognitive control adjustments occurring through an ‘adaptation-by-binding’ which posits that the continuous arousal resulting from a high conflict context strengthens active task and sensory representations even if disadvantageous to automatic processes (Verguts & Notebaert, 2009). Further, ongoing synchronous cortical alpha-band oscillations could serve as a potential neural mechanism by which this binding effect is achieved

The Impact of Cortical State on Neural Coding and Behavior

The brain is never truly silent – up to 80% of its energy budget is expended during ongoing activity in the absence of sensory input. Previous research has shown that sensory neurons are not exclusively influenced by external stimuli but rather reflect interactions between sensory inputs and the ongoing activity of the brain. Yet, whether fluctuations in the state of cortical networks influence sensory coding in neural circuits and the behavior of the animal are unknown. To shed light on this issue, we conducted multi-unit electrophysiology experiments in visual areas V1 and V4 of behaving monkeys. First, we studied the impact of neural population spiking before stimulus presentation on orientation discrimination in the primary visual cortex. We found that when neuronal populations are in a low firing state, they have a higher capacity to discriminate stimulus features despite an overall reduction in evoked responses. Importantly, behavioral performance was significantly improved in the low firing network state. Next, we conducted recordings in the visual cortical area V4 while animals participated in a natural image orientation discrimination task to determine whether fluctuations in local population synchrony during wakefulness play any role in modulating network and behavioral performance. We found that populations of cells exhibit rapid fluctuations in synchrony of ongoing activity ranging from desynchronized responses, indicative of high alertness, to more synchronized responses, indicative of drowsiness. These state fluctuations control the variability in the accuracy of population coding and behavioral performance across trials in a visual discrimination task. When the local population activity is desynchronized, the correlated variability between neurons is reduced, and network and behavioral performance are improved. Lastly, we controlled the state of cortical networks by manipulating the animal’s behavioral state from wakefulness to rest. Thus, we analyzed population recordings from area V4 while the animals participated in an orientation discrimination task, which was immediately followed by a brief resting period of 20-30 minutes, and lastly, by a second task period (Task – Rest – Task). We found that cortical networks were desynchronized after rest such that behavioral performance was improved relative to the pre-rest condition. Altogether, the findings in this thesis demonstrate that the variability in spontaneous cortical activity is not simply noise but rather contains a dynamic structure which controls how incoming sensory information is optimally integrated with ongoing processes to guide network coding and behavior

Alpha Rhythms Reveal When and Where Item and Associative Memories Are Retrieved

Memories for past experiences can range from vague recognition to full-blown recall of associated details. Electroencephalography has shown that recall signals unfold a few hundred milliseconds after simple recognition, but has only provided limited insights into the underlying brain networks. Functional magnetic resonance imaging (fMRI) has revealed a “core recollection network” (CRN) centered on posterior parietal and medial temporal lobe regions, but the temporal dynamics of these regions during retrieval remain largely unknown. Here we used Magnetoencephalography in a memory paradigm assessing correct rejection (CR) of lures, item recognition (IR) and associative recall (AR) in human participants of both sexes. We found that power decreases in the alpha frequency band (10–12 Hz) systematically track different mnemonic outcomes in both time and space: Over left posterior sensors, alpha power decreased in a stepwise fashion from 500 ms onward, first from CR to IR and then from IR to AR. When projecting alpha power into source space, the CRN known from fMRI studies emerged, including posterior parietal cortex (PPC) and hippocampus. While PPC showed a monotonic change across conditions, hippocampal effects were specific to recall. These region-specific effects were corroborated by a separate fMRI dataset. Importantly, alpha power time courses revealed a temporal dissociation between item and associative memory in hippocampus and PPC, with earlier AR effects in hippocampus. Our data thus link engagement of the CRN to the temporal dynamics of episodic memory and highlight the role of alpha rhythms in revealing when and where different types of memories are retrieved

Investigating the neural mechanisms underlying auditory and audio-visual perception in younger and older adults

This thesis aimed to address questions in two distinct areas of research in ageing and cognitive neuroscience. Firstly, given that the pre-stimulus state of cortical oscillations had been shown to predict behavioural and neural responses, we addressed the question of whether pre-stimulus oscillatory mechanisms change or remain consistent in the ageing brain. Secondly, previous research had shown that Audio-visual (AV) speech influences the amplitude and latency of evoked activity. Our research addressed the questions of whether/how AV enhancement and visual predictability of AV speech is represented in evoked activity in noisy listening conditions, and whether such Electroencephalographic (EEG) signatures remain stable with age. In Chapter 3 we investigated the consistency of how pre-stimulus activity influences auditory frequency discrimination performance in young and older participants. In both groups the power of pre-stimulus activity influenced the encoding of sensory evidence reflected by early evoked components, while the phase influenced choice formation in later-activated EEG components. Importantly, for the early EEG components we did not find evidence for a systematic difference in the time scales of the perceptually relevant pre-stimulus activity. In the later-activated EEG component we found a trend for perceptually relevant rhythmic activity to arise from slower frequencies in the ageing brain. At the same time our data replicate previous findings of a significant age-related slowing of Auditory Evoked Potential (AEP) latency, modulations of AEP amplitudes, and a flattening of the spectral profile of EEG activity. In Chapter 4, we investigated the consistency of behaviour and evoked activity underlying AV speech integration in a speech-in-noise discrimination task in younger and older adults. Behaviourally, younger and older adults performed comparably. Performance was greater for Audio-visually informative (AVinf) speech compared to Auditory-only informative (AOinf) speech across groups and noise levels, and was poorer at low noise levels. AV enhancement was greater in high noise levels, across all participants, and older adults derived greater AV enhancement compared to younger adults (an effect that was consistent across noise levels). In terms of visual predictability, we found that word discrimination performance was greater for target words with non-labial initial phonemes (assumed least visually predictive), compared to labial initial phonemes (assumed most visually predictive). Furthermore, we found that AV enhancement was greater for labial initial phonemes, compared to non-labial initial phonemes, and this was consistent across age groups.Neurally, we found that AV enhancement is represented by a centro-parietal P3-like activity in older adults and an N4-like fronto-central activity in younger adults, but found that this activity did not correlate with behavioural AV enhancement. Our results point to distinct patterns of late evoked activity underlying AV enhancement between younger and older adults, possibly representing distinct cognitive (memory) strategies in predicting upcoming target stimuli. At the same time our data replicate previous findings of a significant age-related slowing of AEP latency, modulations of AEP amplitudes, and a flattening of the spectral profile of EEG activity. In Chapter 5 we investigated the consistency of evoked activity underlying the visual predictability of AV speech. We found that visual predictability was reflected by late fronto-central negativity in older adults, but not in younger adults. However, we did not find evidence of an interaction between visual predictability and AV enhancement in terms of evoked activity, raising further questions about how visual predictability of speech is represented the brain’s electrophysiology. Our results point to distinct patterns of late evoked activity underlying visual predictability of visual speech, again possibly reflecting differential strategies in predictive coding. In summary, the results of this thesis demonstrate that pre-stimulus mechanisms in auditory pitch perception remain consistent in the younger and older adult brain, while spectral dynamics change with age. Our results also replicate previous work demonstrating age-related delays in peak latency, and changes in peak amplitude, of early auditory evoked activity. And lastly, we demonstrate that differences in the EEG signatures of AV enhancement between younger and older adults emerge in late evoked activity, and that visual predictability of speech is represented in late evoked activity only in older adults