Bursting with Potential: How Sensorimotor Beta Bursts Develop from Infancy to Adulthood.

Beta activity is thought to play a critical role in sensorimotor processes. However, little is known about how activity in this frequency band develops. Here, we investigated the developmental trajectory of sensorimotor beta activity from infancy to adulthood. We recorded EEG from 9-month-old, 12-month-old, and adult humans (male and female) while they observed and executed grasping movements. We analyzed "beta burst" activity using a novel method that combines time-frequency decomposition and principal component analysis. We then examined the changes in burst rate and waveform motifs along the selected principal components. Our results reveal systematic changes in beta activity during action execution across development. We found a decrease in beta burst rate during movement execution in all age groups, with the greatest decrease observed in adults. Additionally, we identified three principal components that defined waveform motifs that systematically changed throughout the trial. We found that bursts with waveform shapes closer to the median waveform were not rate-modulated, whereas those with waveform shapes further from the median were differentially rate-modulated. Interestingly, the decrease in the rate of certain burst motifs occurred earlier during movement and was more lateralized in adults than in infants, suggesting that the rate modulation of specific types of beta bursts becomes increasingly refined with age.SIGNIFICANCE STATEMENT We demonstrate that, like in adults, sensorimotor beta activity in infants during reaching and grasping movements occurs in bursts, not oscillations like thought traditionally. Furthermore, different beta waveform shapes were differentially modulated with age, including more lateralization in adults. Aberrant beta activity characterizes various developmental disorders and motor difficulties linked to early brain injury, so looking at burst waveform shape could provide more sensitivity for early identification and treatment of affected individuals before any behavioral symptoms emerge. More generally, comparison of beta burst activity in typical versus atypical motor development will also be instrumental in teasing apart the mechanistic functional roles of different types of beta bursts.

Bayesian multilevel hidden Markov models identify stable state dynamics in longitudinal recordings from macaque primary motor cortex.

Neural populations, rather than single neurons, may be the fundamental unit of cortical computation. Analysing chronically recorded neural population activity is challenging not only because of the high dimensionality of activity but also because of changes in the signal that may or may not be due to neural plasticity. Hidden Markov models (HMMs) are a promising technique for analysing such data in terms of discrete latent states, but previous approaches have not considered the statistical properties of neural spiking data, have not been adaptable to longitudinal data, or have not modelled condition-specific differences. We present a multilevel Bayesian HMM addresses these shortcomings by incorporating multivariate Poisson log-normal emission probability distributions, multilevel parameter estimation and trial-specific condition covariates. We applied this framework to multi-unit neural spiking data recorded using chronically implanted multi-electrode arrays from macaque primary motor cortex during a cued reaching, grasping and placing task. We show that, in line with previous work, the model identifies latent neural population states which are tightly linked to behavioural events, despite the model being trained without any information about event timing. The association between these states and corresponding behaviour is consistent across multiple days of recording. Notably, this consistency is not observed in the case of a single-level HMM, which fails to generalise across distinct recording sessions. The utility and stability of this approach is demonstrated using a previously learned task, but this multilevel Bayesian HMM framework would be especially suited for future studies of long-term plasticity in neural populations.

Longitudinal effects of early psychosocial deprivation on macaque executive function: Evidence from computational modelling.

Executive function (EF) describes a group of cognitive processes underlying the organization and control of goal-directed behaviour. Environmental experience appears to play a crucial role in EF development, with early psychosocial deprivation often linked to EF impairment. However, many questions remain concerning the developmental trajectories of EF after exposure to deprivation, especially concerning specific mechanisms. Accordingly, using an 'A-not-B' paradigm and a macaque model of early psychosocial deprivation, we investigated how early deprivation influences EF development longitudinally from adolescence into early adulthood. The contribution of working memory and inhibitory control mechanisms were examined specifically via the fitting of a computational model of decision making to the choice behaviour of each individual. As predicted, peer-reared animals (i.e. those exposed to early psychosocial deprivation) performed worse than mother-reared animals across time, with the fitted model parameters yielding novel insights into the functional decomposition of group-level EF differences underlying task performance. Results indicated differential trajectories of inhibitory control and working memory development in the two groups. Such findings not only extend our knowledge of how early deprivation influences EF longitudinally, but also provide support for the utility of computational modelling to elucidate specific mechanisms linking early psychosocial deprivation to long-term poor outcomes.

Perturbation of Right Dorsolateral Prefrontal Cortex Makes Power Holders Less Resistant to Tempting Bribes.

Bribery is a common form of corruption that takes place when a briber suborns a power holder to achieve an advantageous outcome at the cost of moral transgression. Although bribery has been extensively investigated in the behavioral sciences, its underlying neurobiological basis remains poorly understood. Here, we employed transcranial direct-current stimulation (tDCS) in combination with a novel paradigm (N = 119 adults) to investigate whether disruption of right dorsolateral prefrontal cortex (rDLPFC) causally changed bribe-taking decisions of power holders. Perturbing rDLPFC via tDCS specifically made participants more willing to take bribes as the relative value of the offer increased. This tDCS-induced effect could not be explained by changes in other measures. Model-based analyses further revealed that such neural modulation alters the concern for generating profits for oneself via taking bribes and reshapes the concern for the distribution inequity between oneself and the briber, thereby influencing the subsequent decisions. These findings reveal a causal role of rDLPFC in modulating corrupt behavior.

Laminar dynamics of high amplitude beta bursts in human motor cortex.

Motor cortical activity in the beta frequency range is one of the strongest and most studied movement-related neural signals. At the single trial level, beta band activity is often characterized by transient, high amplitude, bursting events rather than slowly modulating oscillations. The timing of these bursting events is tightly linked to behavior, suggesting a more dynamic functional role for beta activity than previously believed. However, the neural mechanisms underlying beta bursts in sensorimotor circuits are poorly understood. To address this, we here leverage and extend recent developments in high precision MEG for temporally resolved laminar analysis of burst activity, combined with a neocortical circuit model that simulates the biophysical generators of the electrical currents which drive beta bursts. This approach pinpoints the generation of beta bursts in human motor cortex to distinct excitatory synaptic inputs to deep and superficial cortical layers, which drive current flow in opposite directions. These laminar dynamics of beta bursts in motor cortex align with prior invasive animal recordings within the somatosensory cortex, and suggest a conserved mechanism for somatosensory and motor cortical beta bursts. More generally, we demonstrate the ability for uncovering the laminar dynamics of event-related neural signals in human non-invasive recordings. This provides important constraints to theories about the functional role of burst activity for movement control in health and disease, and crucial links between macro-scale phenomena measured in humans and micro-circuit activity recorded from animal models.

Estimates of cortical column orientation improve MEG source inversion.

Determining the anatomical source of brain activity non-invasively measured from EEG or MEG sensors is challenging. In order to simplify the source localization problem, many techniques introduce the assumption that current sources lie on the cortical surface. Another common assumption is that this current flow is orthogonal to the cortical surface, thereby approximating the orientation of cortical columns. However, it is not clear which cortical surface to use to define the current source locations, and normal vectors computed from a single cortical surface may not be the best approximation to the orientation of cortical columns. We compared three different surface location priors and five different approaches for estimating dipole vector orientation, both in simulations and visual and motor evoked MEG responses. We show that models with source locations on the white matter surface and using methods based on establishing correspondences between white matter and pial cortical surfaces dramatically outperform models with source locations on the pial or combined pial/white surfaces and which use methods based on the geometry of a single cortical surface in fitting evoked visual and motor responses. These methods can be easily implemented and adopted in most M/EEG analysis pipelines, with the potential to significantly improve source localization of evoked responses.

High-precision magnetoencephalography for reconstructing amygdalar and hippocampal oscillations during prediction of safety and threat.

Learning to associate neutral with aversive events in rodents is thought to depend on hippocampal and amygdala oscillations. In humans, oscillations underlying aversive learning are not well characterised, largely due to the technical difficulty of recording from these two structures. Here, we used high-precision magnetoencephalography (MEG) during human discriminant delay threat conditioning. We constructed generative anatomical models relating neural activity with recorded magnetic fields at the single-participant level, including the neocortex with or without the possibility of sources originating in the hippocampal and amygdalar structures. Models including neural activity in amygdala and hippocampus explained MEG data during threat conditioning better than exclusively neocortical models. We found that in both amygdala and hippocampus, theta oscillations during anticipation of an aversive event had lower power compared to safety, both during retrieval and extinction of aversive memories. At the same time, theta synchronisation between hippocampus and amygdala increased over repeated retrieval of aversive predictions, but not during safety. Our results suggest that high-precision MEG is sensitive to neural activity of the human amygdala and hippocampus during threat conditioning and shed light on the oscillation-mediated mechanisms underpinning retrieval and extinction of fear memories in humans.

Non-invasive laminar inference with MEG: Comparison of methods and source inversion algorithms.

Magnetoencephalography (MEG) is a direct measure of neuronal current flow; its anatomical resolution is therefore not constrained by physiology but rather by data quality and the models used to explain these data. Recent simulation work has shown that it is possible to distinguish between signals arising in the deep and superficial cortical laminae given accurate knowledge of these surfaces with respect to the MEG sensors. This previous work has focused around a single inversion scheme (multiple sparse priors) and a single global parametric fit metric (free energy). In this paper we use several different source inversion algorithms and both local and global, as well as parametric and non-parametric fit metrics in order to demonstrate the robustness of the discrimination between layers. We find that only algorithms with some sparsity constraint can successfully be used to make laminar discrimination. Importantly, local t-statistics, global cross-validation and free energy all provide robust and mutually corroborating metrics of fit. We show that discrimination accuracy is affected by patch size estimates, cortical surface features, and lead field strength, which suggests several possible future improvements to this technique. This study demonstrates the possibility of determining the laminar origin of MEG sensor activity, and thus directly testing theories of human cognition that involve laminar- and frequency-specific mechanisms. This possibility can now be achieved using recent developments in high precision MEG, most notably the use of subject-specific head-casts, which allow for significant increases in data quality and therefore anatomically precise MEG recordings. SECTION: Analysis methods. CLASSIFICATIONS: Source localization: inverse problem; Source localization: other.

Effects of Infant Cleft Lip on Adult Gaze and Perceptions of "Cuteness".

OBJECTIVE: Early mother-infant interactions are impaired in the context of infant cleft lip and are associated with adverse child psychological outcomes, but the nature of these interaction difficulties is not yet fully understood. The aim of this study was to explore adult gaze behavior and cuteness perception, which are particularly important during early social exchanges, in response to infants with cleft lip, in order to investigate potential foundations for the interaction difficulties seen in this population. METHODS: Using an eye tracker, eye movements were recorded as adult participants viewed images of infant faces with and without cleft lip. Participants also rated each infant on a scale of cuteness. RESULTS: Participants fixated significantly longer on the mouths of infants with cleft lip, which occurred at the expense of fixation on eyes. Severity of cleft lip was associated with the strength of fixation bias, with participants looking even longer at the mouths of infants with the most severe clefts. Infants with cleft lip were rated as significantly less cute than unaffected infants. Men rated infants as less cute than women overall but gave particularly low ratings to infants with cleft lip. CONCLUSIONS: Results demonstrate that the limited disturbance in infant facial configuration of cleft lip can significantly alter adult gaze patterns and cuteness perception. Our findings could have important implications for early interactions and may help in the development of interventions to foster healthy development in infants with cleft lip.

Beta bursts question the ruling power for brain-computer interfaces.

Objective: Current efforts to build reliable brain-computer interfaces (BCI) span multiple axes from hardware, to software, to more sophisticated experimental protocols, and personalized approaches. However, despite these abundant efforts, there is still room for significant improvement. We argue that a rather overlooked direction lies in linking BCI protocols with recent advances in fundamental neuroscience.Approach: In light of these advances, and particularly the characterization of the burst-like nature of beta frequency band activity and the diversity of beta bursts, we revisit the role of beta activity in 'left vs. right hand' motor imagery (MI) tasks. Current decoding approaches for such tasks take advantage of the fact that MI generates time-locked changes in induced power in the sensorimotor cortex and rely on band-passed power changes in single or multiple channels. Although little is known about the dynamics of beta burst activity during MI, we hypothesized that beta bursts should be modulated in a way analogous to their activity during performance of real upper limb movements.Main results and Significance: We show that classification features based on patterns of beta burst modulations yield decoding results that are equivalent to or better than typically used beta power across multiple open electroencephalography datasets, thus providing insights into the specificity of these bio-markers.

High precision magnetoencephalography reveals increased right-inferior frontal gyrus beta power during response conflict.

Flexibility of behavior and the ability to rapidly switch actions is critical for adaptive living in humans. It is well established that the right-inferior frontal gyrus (R-IFG) is recruited during outright action-stopping, relating to increased beta (12-30 Hz) power. It has also been posited that inhibiting incorrect response tendencies and switching is central to motor flexibility. However, it is not known if the commonly reported R-IFG beta signature of response inhibition in action-stopping is also recruited during response conflict, which would suggest overlapping networks for stopping and switching. In the current study, we analyzed high precision magnetoencephalography (hpMEG) data recorded with multiple within subject recording sessions (trials n > 10,000) from 8 subjects during different levels of response conflict. We hypothesized that a R-IFG-triggered network for response inhibition is domain general and therefore also involved in mediating response conflict. We tested whether R-IFG showed increased beta power dependent on the level of response conflict. Using event-related spectral perturbations and linear mixed modeling, we found that R-IFG beta power increased for response conflict trials. The R-IFG beta increase was specific to trials with strong response conflict, and increased R-IFG beta power related to less error. This supports a more generalized role for R-IFG beta, beyond simple stopping behavior towards response switching.

Diverse beta burst waveform motifs characterize movement-related cortical dynamics.

Classical analyses of induced, frequency-specific neural activity typically average band-limited power over trials. More recently, it has become widely appreciated that in individual trials, beta band activity occurs as transient bursts rather than amplitude-modulated oscillations. Most studies of beta bursts treat them as unitary, and having a stereotyped waveform. However, we show there is a wide diversity of burst shapes. Using a biophysical model of burst generation, we demonstrate that waveform variability is predicted by variability in the synaptic drives that generate beta bursts. We then use a novel, adaptive burst detection algorithm to identify bursts from human MEG sensor data recorded during a joystick-based reaching task, and apply principal component analysis to burst waveforms to define a set of dimensions, or motifs, that best explain waveform variance. Finally, we show that bursts with a particular range of waveform motifs, ones not fully accounted for by the biophysical model, differentially contribute to movement-related beta dynamics. Sensorimotor beta bursts are therefore not homogeneous events and likely reflect distinct computational processes.

Spatiotemporal organisation of human sensorimotor beta burst activity.

Beta oscillations in human sensorimotor cortex are hallmark signatures of healthy and pathological movement. In single trials, beta oscillations include bursts of intermittent, transient periods of high-power activity. These burst events have been linked to a range of sensory and motor processes, but their precise spatial, spectral, and temporal structure remains unclear. Specifically, a role for beta burst activity in information coding and communication suggests spatiotemporal patterns, or travelling wave activity, along specific anatomical gradients. We here show in human magnetoencephalography recordings that burst activity in sensorimotor cortex occurs in planar spatiotemporal wave-like patterns that dominate along two axes either parallel or perpendicular to the central sulcus. Moreover, we find that the two propagation directions are characterised by distinct anatomical and physiological features. Finally, our results suggest that sensorimotor beta bursts occurring before and after a movement can be distinguished by their anatomical, spectral, and spatiotemporal characteristics, indicating distinct functional roles.

Detection and analysis of cortical beta bursts in developmental EEG data.

Developmental EEG research often involves analyzing signals within various frequency bands, based on the assumption that these signals represent oscillatory neural activity. However, growing evidence suggests that certain frequency bands are dominated by transient burst events in single trials rather than sustained oscillations. This is especially true for the beta band, with adult 'beta burst' timing a better predictor of motor behavior than slow changes in average beta amplitude. No developmental research thus far has looked at beta bursts, with techniques used to investigate frequency-specific activity structure rarely even applied to such data. Therefore, we aimed to: i) provide a tutorial for developmental EEG researchers on the application of methods for evaluating the rhythmic versus transient nature of frequency-specific activity; and ii) use these techniques to investigate the existence of sensorimotor beta bursts in infants. We found that beta activity in 12-month-olds did occur in bursts, however differences were also revealed in terms of duration, amplitude, and rate during grasping compared to adults. Application of the techniques illustrated here will be critical for clarifying the functional roles of frequency-specific activity across early development, including the role of beta activity in motor processing and its contribution to differing developmental motor trajectories.

Building blocks of joint attention: Early sensitivity to having one's own gaze followed.

Detecting when one's own gaze has been followed is a critical component of joint attention, but little is known about its development. To address this issue, we used electroencephalography (EEG) to record infant neural responses at 6.5 and 9.5 months during observation of an adult either turning to look at the same object as the infant (congruent actor), or turning to look at a different object (incongruent actor). We also used a preferential looking paradigm to investigate whether infants would demonstrate a preference for the congruent versus incongruent actor. Greater suppression of alpha band activity in the congruent compared to incongruent condition was revealed at both ages in central and parietal regions. However, the effect of congruency on alpha suppression was stronger at 9.5 months, and only at this age did infants demonstrate a preference towards looking at the congruent actor. Together, these results suggest that although infants are sensitive to others' gaze following from early on, important neural and behavioural developments occur between 6.5 and 9.5 months.

Lamina-specific cortical dynamics in human visual and sensorimotor cortices.

Distinct anatomical and spectral channels are thought to play specialized roles in the communication within cortical networks. While activity in the alpha and beta frequency range (7 - 40 Hz) is thought to predominantly originate from infragranular cortical layers conveying feedback-related information, activity in the gamma range (>40 Hz) dominates in supragranular layers communicating feedforward signals. We leveraged high precision MEG to test this proposal, directly and non-invasively, in human participants performing visually cued actions. We found that visual alpha mapped onto deep cortical laminae, whereas visual gamma predominantly occurred more superficially. This lamina-specificity was echoed in movement-related sensorimotor beta and gamma activity. These lamina-specific pre- and post- movement changes in sensorimotor beta and gamma activity suggest a more complex functional role than the proposed feedback and feedforward communication in sensory cortex. Distinct frequency channels thus operate in a lamina-specific manner across cortex, but may fulfill distinct functional roles in sensory and motor processes.

Response repetition biases in human perceptual decisions are explained by activity decay in competitive attractor models.

Animals and humans have a tendency to repeat recent choices, a phenomenon known as choice hysteresis. The mechanism for this choice bias remains unclear. Using an established, biophysically informed model of a competitive attractor network for decision making, we found that decaying tail activity from the previous trial caused choice hysteresis, especially during difficult trials, and accurately predicted human perceptual choices. In the model, choice variability could be directionally altered through amplification or dampening of post-trial activity decay through simulated depolarizing or hyperpolarizing network stimulation. An analogous intervention using transcranial direct current stimulation (tDCS) over left dorsolateral prefrontal cortex (dlPFC) yielded a close match between model predictions and experimental results: net soma depolarizing currents increased choice hysteresis, while hyperpolarizing currents suppressed it. Residual activity in competitive attractor networks within dlPFC may thus give rise to biases in perceptual choices, which can be directionally controlled through non-invasive brain stimulation.

Understanding the nonlinear physiological and behavioral effects of tDCS through computational neurostimulation.

Despite the success of noninvasive brain stimulation (NIBS), the mechanism of action through which different stimulation techniques interact with information processing in targeted neural circuits largely remains unknown. Applying neurostimulation in silico to computational models with biophysical plausibility provides one route to interrogate the possible mechanisms through which stimulation interacts with neural circuits, and generate predictions about the resultant behavior. Here, we address the recent observation that the physiological and behavioral effects of transcranial direct current stimulation (tDCS) might be nonlinear with regard to stimulation intensity or duration. We simulate neurostimulation in an established, biophysically informed neural network attractor model that generates simple behavioral choices and thus allows for assessing the impact of stimulation on both neural dynamics and behavior. We demonstrate that nonlinear effects of stimulation intensity on the accuracy and decision time of the model can arise from a limit on the integration rate of the network, nonlinear effects of stimulation on neural firing rates before the onset of the stimulus, and the inhibitory effect of hyperpolarizing stimulation on pyramidal neurons. We thus present a detailed modeling treatment of nonlinear tDCS effects during a behavioral task, and provide detailed hypotheses about the neural causes that lead to observed nonlinear behavioral effects during stimulation. This framework can provide a blueprint for future work on the neural and behavioral consequences of NIBS in health and disease.

Action and language mechanisms in the brain: data, models and neuroinformatics.

We assess the challenges of studying action and language mechanisms in the brain, both singly and in relation to each other to provide a novel perspective on neuroinformatics, integrating the development of databases for encoding ­ separately or together ­ neurocomputational models and empirical data that serve systems and cognitive neuroscience.