The neurophysiology of intersensory selective attention and task switching

Our ability to selectively attend to certain aspects of the world and ignore others is fundamental to our day-to-day lives. The need for selective attention stems from capacity limitations inherent in our perceptual and cognitive processing architecture. Because not every elemental piece of our environment can be fully processed in parallel, the nervous system must prioritize processing. This prioritization is generally referred to as selective attention. Meanwhile, we are faced with a world that is constantly in flux, such that we have to frequently shift our attention from one piece of the environment to another and from one task to another. This process is generally referred to as task-switching. Neural oscillations in the alpha band (~8-14 Hz) have been shown to index the distribution of selective attention, and there is increasing evidence that oscillations in this band are in fact utilized by the nervous system to suppress distracting, task-irrelevant information. In order to elaborate on what is known of the function of alpha oscillations as well as current models of both intersensory selective attention and task switching, I investigated the dynamics of alpha amplitude modulations within the context of intersenory selective attention and task switching in neurologically typical young adults. Participants were alternately cued to attend to either the visual or auditory aspect of a compound audio-visual stimulus while high-density electroencephalography was recorded. It is typically found that alpha power increases over parieto-occipital cortices when attention is directed away from the visual modality and to the auditory modality. I report evidence that alpha oscillations play a role in task-switching (e.g., when switching from attending the visual task versus repeating this task), specifically as biasing signals, that may operate to re-weight competition among two tasks-sets. I further investigated the development of these same processes in school-aged children and adolescents. While exhibiting typical patterns of alpha modulations relevant to selective attention, Young school-aged children (8-12 years), compared to older participants, did not demonstrate specific task switching modulation of alpha oscillations, suggesting that this process does not fully develop until late adolescence. Finally, children and adolescents on the autism spectrum failed altogether to exhibit differentiation of alpha power between attend-visual and attend-auditory conditions--an effect present in age and IQ matched controls--suggesting that ASD individuals may have a deficit in the overall top-down deployment of alpha oscillatory biasing signals. This could result in an inability to ignore distracting information in the environment, leading to an overwhelming, disordered experience of the world, resulting in profound effects on the both social interaction and cognitive development. Altogether, these findings add to growing evidence that alpha oscillations serve as domain general biasing signals and are integral to our flexible goal-oriented behavior. Furthermore, the flexible use of these biasing signals in selective attention and task switching develops over a protracted period, and appears to be aberrant in autism spectrum disorder

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

Brain oscillatory correlates in working memory and attentional control processes

Human working memory and selective attention processes in need of top-down cognitive control rely on interactions within local neural populations and between distant brain areas in a fronto-parietal neural network. Brain oscillatory dynamics drawing on slow oscillatory activity in the theta frequency range are associated with (1) information exchange between global and local networks needed for the integration of top-down controlled mental templates and bottom-up visual processing, through transient phase-synchronization with fast gamma activity, (2) the prefrontal top-down control of remote brain areas, where frontal-midline theta phase may provide cyclic windows of opportunity in which task-active posterior areas can access prefrontal resources, or are denied access and (3) the coordination of excitable periods within the fronto-parietal network, through long-range theta coherence. In this thesis, four research projects are presented. In a newly developed visual search task, we demonstrated that in conditions where participants kept a single targets' properties in mind for visual search, cross-frequency synchronization between theta and gamma phase transiently increased in right posterior cortex, but not in conditions where one out of multiple mental templates was successfully matched. Thereby, we extend previous work proposing transient theta-gamma phase synchronization as a neural correlate of matching incoming sensory information with top-down controlled mental templates, and we provide novel evidence for limitations in memory matching during multiple template search. Second, we probed the causal relevance of more sustained fronto-parietal interaction, during voluntary resource allocation in visuospatial working memory. We found frontal-midline theta phase dependent effects of TMS over right, but not left, parietal cortex on working memory performance, when prioritizing contralateral visuospatial information during working memory maintenance. TMS selectively disrupted task accuracy when delivered during the more excitatory frontal-midline theta phase (i.e. the trough). Based on this pilot data, we recommend effect size estimates and implications for follow-up studies. Third, we conducted a pre-registered study using multi-site theta tACS for synchronizing or desynchronizing a left fronto-parietal network, but could not reproduce a beneficial or detrimental effect on verbal working memory performance in an easy letter recognition task. Our results indicate that a beneficial effect of synchronous fronto-parietal theta tACS can only be observed in a working memory task of high difficulty. In order to make our contribution to increasing reproducibility and robustness in transcranial brain stimulation research, we next investigated the usefulness of Bayes Factor analyses over conventional tests to differentiate between cases where a particular application of TBS had no effect or whether results were merely inconclusive. In a series of simulated TBS experiments with differing sample size and effect size, we show that Bayes factors tests may be highly useful for demonstrating conclusive evidence for non-effects and outline how they can be used in practice

Altered Alpha Oscillatory Power Dynamics Underlie Difficulties with Cognitive Flexibility

Cognitive flexibility is an important mental faculty, but there are certain populations that experience reduced flexibility, which may be associated with altered neural activity. Rumination is when an individual becomes mentally stuck on a thought, and they experience difficulty shifting their attention away from the ruminative thought demonstrating reduced cognitive flexibility. In a similar manner, individuals diagnosed with substance use disorder show varying degrees of attentional bias towards drug related stimuli. The drug cues capture attention, and it is difficult for these individuals to shift attention away from thoughts related to drug cues. Both populations experience difficulty shifting attention when they experience highly salient thoughts (high automatic constraints). Here we suggest and demonstrate that reduced cognitive flexibility in these populations is associated with altered activity of alpha oscillations, as alpha oscillations play an important role in supporting cognitive flexibility. In our first study, we assess the relationship between trait tendency to ruminate and resting state alpha power in left frontal and parietal located electrodes. Individuals higher in trait rumination exhibit higher alpha power in left frontal located electrodes. This finding suggests that higher alpha power may contribute to mental inflexibility associated with rumination. In our second study, we assess the relationship between attentional bias towards drug cues and alpha power while automatic constraints on thought are high during an emotional version of the Stroop task and when drug cues are not present and therefore automatic constraints are low, but flexibility is required during a probabilistic reversal learning task. The emotional version of the Stroop task includes traditional congruent and incongruent word meanings as well as drug related and neutral word meanings. Participants in this study were long-term nicotine smokers, therefore the emotional stimuli were smoking related. The probabilistic reversal learning task instructs participants to choose one of two presented stimuli on each trial. The stimuli have different probabilities of reward or punishment. If the participant chooses the stimulus with the higher probability of reward several trials in a row, the reward probabilities reverse, and the participant must adapt to the new reward contingencies. Participants demonstrate the traditional Stroop effect of lower accuracy and slower reaction time during incongruent trials compared to congruent trials. Additionally, participants show a slowed reaction time during drug trials compared to neutral trials suggesting attentional bias during drug trials. Greater attentional bias is associated with higher alpha power in left frontal electrodes during drug trials. No significant relationship between attentional bias and alpha power during the probabilistic reversal learning task was revealed. Together, these results suggest higher alpha power in left frontal regions may contribute to mental inflexibility prompted by attentional bias when automatic constraints are high, but when automatic constraints are low, flexibility may not be reduced. All together these results reveal a relationship between reduced cognitive flexibility when salient stimuli or thoughts are present and altered alpha power dynamics, which may offer new avenues for behavioral intervention to improve cognitive flexibility

Modeling biophysical and neural circuit bases for core cognitive abilities evident in neuroimaging patterns: hippocampal mismatch, mismatch negativity, repetition positivity, and alpha suppression of distractors

This dissertation develops computational models to address outstanding problems in the domain of expectation-related cognitive processes and their neuroimaging markers in functional MRI or EEG. The new models reveal a way to unite diverse phenomena within a common framework focused on dynamic neural encoding shifts, which can arise from robust interactive effects of M-currents and chloride currents in pyramidal neurons. By specifying efficient, biologically realistic circuits that achieve predictive coding (e.g., Friston, 2005), these models bridge among neuronal biophysics, systems neuroscience, and theories of cognition. Chapter one surveys data types and neural processes to be examined, and outlines the Dynamically Labeled Predictive Coding (DLPC) framework developed during the research. Chapter two models hippocampal prediction and mismatch, using the DLPC framework. Chapter three presents extensions to the model that allow its application for modeling neocortical EEG genesis. Simulations of this extended model illustrate how dynamic encoding shifts can produce Mismatch Negativity (MMN) phenomena, including pharmacological effects on MMN reported for humans or animals. Chapters four and five describe new modeling studies of possible neural bases for alpha-induced information suppression, a phenomenon associated with active ignoring of stimuli. Two models explore the hypothesis that in simple rate-based circuits, information suppression might be a robust effect of neural saturation states arising near peaks of resonant alpha oscillations. A new proposal is also introduced for how the basal ganglia may control onset and offset of alpha-induced information suppression. Although these rate models could reproduce many experimental findings, they fell short of reproducing a key electrophysiological finding: phase-dependent reduction in spiking activity correlated with power in the alpha frequency band. Therefore, chapter five also specifies how a DLPC model, adapted from the neocortical model developed in chapter three, can provide an expectation-based model of alpha-induced information suppression that exhibits phase-dependent spike reduction during alpha-band oscillations. The model thus can explain experimental findings that were not reproduced by the rate models. The final chapter summarizes main theses, results, and basic research implications, then suggests future directions, including expanded models of neocortical mismatch, applications to artificial neural networks, and the introduction of reward circuitry

Task switching in the prefrontal cortex

The overall goal of this dissertation is to elucidate the cellular and circuit mechanisms underlying flexible behavior in the prefrontal cortex. We are often faced with situations in which the appropriate behavior in one context is inappropriate in others. If these situations are familiar, we can perform the appropriate behavior without relearning how the context relates to the behavior — an important hallmark of intelligence. Neuroimaging and lesion studies have shown that this dynamic, flexible process of remapping context to behavior (task switching) is dependent on prefrontal cortex, but the precise contributions and interactions of prefrontal subdivisions are still unknown. This dissertation investigates two prefrontal areas that are thought to be involved in distinct, but complementary executive roles in task switching — the dorsolateral prefrontal cortex (dlPFC) and the anterior cingulate cortex (ACC). Using electrophysiological recordings from macaque monkeys, I show that synchronous network oscillations in the dlPFC provide a mechanism to flexibly coordinate context representations (rules) between groups of neurons during task switching. Then, I show that, wheras the ACC neurons can represent rules at the cellular level, they do not play a significant role in switching between contexts — rather they seem to be more related to errors and motivational drive. Finally, I develop a set of web-enabled interactive visualization tools designed to provide a multi-dimensional integrated view of electrophysiological datasets. Taken together, these results contribute to our understanding of task switching by investigating new mechanisms for coordination of neurons in prefrontal cortex, clarifying the roles of prefrontal subdivisions during task switching, and providing visualization tools that enhance exploration and understanding of large, complex and multi-scale electrophysiological data

Nonlinear brain dynamics as macroscopic manifestation of underlying many-body field dynamics

Neural activity patterns related to behavior occur at many scales in time and space from the atomic and molecular to the whole brain. Here we explore the feasibility of interpreting neurophysiological data in the context of many-body physics by using tools that physicists have devised to analyze comparable hierarchies in other fields of science. We focus on a mesoscopic level that offers a multi-step pathway between the microscopic functions of neurons and the macroscopic functions of brain systems revealed by hemodynamic imaging. We use electroencephalographic (EEG) records collected from high-density electrode arrays fixed on the epidural surfaces of primary sensory and limbic areas in rabbits and cats trained to discriminate conditioned stimuli (CS) in the various modalities. High temporal resolution of EEG signals with the Hilbert transform gives evidence for diverse intermittent spatial patterns of amplitude (AM) and phase modulations (PM) of carrier waves that repeatedly re-synchronize in the beta and gamma ranges at near zero time lags over long distances. The dominant mechanism for neural interactions by axodendritic synaptic transmission should impose distance-dependent delays on the EEG oscillations owing to finite propagation velocities. It does not. EEGs instead show evidence for anomalous dispersion: the existence in neural populations of a low velocity range of information and energy transfers, and a high velocity range of the spread of phase transitions. This distinction labels the phenomenon but does not explain it. In this report we explore the analysis of these phenomena using concepts of energy dissipation, the maintenance by cortex of multiple ground states corresponding to AM patterns, and the exclusive selection by spontaneous breakdown of symmetry (SBS) of single states in sequences.Comment: 31 page

Macaque anterior cingulate cortex deactivation impairs performance and alters lateral prefrontal oscillatory activities in a rule-switching task

© 2019 Ma et al. In primates, both the dorsal anterior cingulate cortex (dACC) and the dorsolateral prefrontal cortex (dlPFC) are key regions of the frontoparietal cognitive control network. To study the role of the dACC and its communication with the dlPFC in cognitive control, we recorded local field potentials (LFPs) from the dlPFC before and during the reversible deactivation of the dACC, in macaque monkeys engaging in uncued switches between 2 stimulus-response rules, namely prosaccade and antisaccade. Cryogenic dACC deactivation impaired response accuracy during maintenance of—but not the initial switching to—the cognitively demanding antisaccade rule, which coincided with a reduction in task-related theta activity and the correct-error (C-E) difference in dlPFC beta-band power. During both rule switching and maintenance, dACC deactivation prolonged the animals’ reaction time and reduced task-related alpha power in the dlPFC. Our findings support a role of the dACC in prefrontal oscillatory activities that are involved the maintenance of a new, challenging task rule

Attentional refocusing between time and space in older adults:investigation of neural mechanisms and relation to driving

Older adults have a disproportionately high risk of causing collisions at intersections and causing collisions by failing to notice surrounding road signs or signals. Collisions caused by older drivers seem to result from attentional failures. There is limited research exploring the ability to refocus from orienting attention to events changing in time (i.e. temporal attention) to distributing attention spatially (i.e. spatial attention), a process that is particularly important while driving and, if impaired,could cause collisions. The aims of the project were firstly to assess whether the ability to refocus attention from time to space changes throughout the adult lifespan when assessed with a computer based task and in an ecologically valid scenario during simulated driving, secondly, to use magnetoencephalography (MEG) to identify changes to neural mechanism that might explain difficulties in attentional refocusing, and finally, use mobile electroencephalography to explore the neural mechanisms involved in attentional refocusing while driving. Results demonstrated age related declines in the ability to refocus attention from time to space both in a computer-based task and during simulated driving. MEG recorded in a computer-based attention refocusing task revealed that, compared to younger adults, older and middle-aged adults displayed task-related theta deficits in lower level visual processing areas, and instead, displayed compensatory increases in theta power and phase-related connectivity across frontal regions. Increased frontal lobe recruitment likely reflects enhanced top-down attention to cope with impaired lower level attention mechanisms,supporting compensatory recruitment models of ageing. During simulated driving, older participants displayed slower driving speeds and weaker beta desynchronization in preparation to read a road sign, instead displaying a stronger theta power increase in response to the road sign, further demonstrating neural and behavioural compensatory strategies that are only partially successful.Findings warrant the development of a training programme to improve attentional refocusing between time and space while driving