Cardiac-Sympathetic Contractility and Neural Alpha-Band Power: Cross-Modal Collaboration during Approach-Avoidance Conflict.

As evidence mounts that the cardiac-sympathetic nervous system reacts to challenging cognitive settings, we ask if these responses are epiphenomenal companions or if there is evidence suggesting a more intertwined role of this system with cognitive function. Healthy male and female human participants performed an approach-avoidance paradigm, trading off monetary reward for painful electric shock, while we recorded simultaneous electroencephalographic and cardiac-sympathetic signals. Participants were reward sensitive but also experienced approach-avoidance "conflict" when the subjective appeal of the reward was near equivalent to the revulsion of the cost. Drift-diffusion model parameters suggested that participants managed conflict in part by integrating larger volumes of evidence into choices (wider decision boundaries). Late alpha-band (neural) dynamics were consistent with widening decision boundaries serving to combat reward sensitivity and spread attention more fairly to all dimensions of available information. Independently, wider boundaries were also associated with cardiac "contractility" (an index of sympathetically mediated positive inotropy). We also saw evidence of conflict-specific "collaboration" between the neural and cardiac-sympathetic signals. In states of high conflict, the alignment (i.e., product) of alpha dynamics and contractility were associated with a further widening of the boundary, independent of either signal's singular association. Cross-trial coherence analyses provided additional evidence that the autonomic systems controlling cardiac-sympathetics might influence the assessment of information streams during conflict by disrupting or overriding reward processing. We conclude that cardiac-sympathetic control might play a critical role, in collaboration with cognitive processes, during the approach-avoidance conflict in humans.

Menstrual cycle-driven hormone concentrations co-fluctuate with white and gray matter architecture changes across the whole brain.

Cyclic fluctuations in hypothalamic-pituitary-gonadal axis (HPG-axis) hormones exert powerful behavioral, structural, and functional effects through actions on the mammalian central nervous system. Yet, very little is known about how these fluctuations alter the structural nodes and information highways of the human brain. In a study of 30 naturally cycling women, we employed multidimensional diffusion and T1-weighted imaging during three estimated menstrual cycle phases (menses, ovulation, and mid-luteal) to investigate whether HPG-axis hormone concentrations co-fluctuate with alterations in white matter (WM) microstructure, cortical thickness (CT), and brain volume. Across the whole brain, 17ß-estradiol and luteinizing hormone (LH) concentrations were directly proportional to diffusion anisotropy (µFA; 17ß-estradiol: ß1 = 0.145, highest density interval (HDI) = [0.211, 0.4]; LH: ß1 = 0.111, HDI = [0.157, 0.364]), while follicle-stimulating hormone (FSH) was directly proportional to CT (ß1 = 0 .162, HDI = [0.115, 0.678]). Within several individual regions, FSH and progesterone demonstrated opposing relationships with mean diffusivity (Diso) and CT. These regions mainly reside within the temporal and occipital lobes, with functional implications for the limbic and visual systems. Finally, progesterone was associated with increased tissue (ß1 = 0.66, HDI = [0.607, 15.845]) and decreased cerebrospinal fluid (CSF; ß1 = -0.749, HDI = [-11.604, -0.903]) volumes, with total brain volume remaining unchanged. These results are the first to report simultaneous brain-wide changes in human WM microstructure and CT coinciding with menstrual cycle-driven hormone rhythms. Effects were observed in both classically known HPG-axis receptor-dense regions (medial temporal lobe, prefrontal cortex) and in other regions located across frontal, occipital, temporal, and parietal lobes. Our results suggest that HPG-axis hormone fluctuations may have significant structural impacts across the entire brain.

Sympathetic involvement in time-constrained sequential foraging.

Appraising sequential offers relative to an unknown future opportunity and a time cost requires an optimization policy that draws on a learned estimate of an environment's richness. Converging evidence points to a learning asymmetry, whereby estimates of this richness update with a bias toward integrating positive information. We replicate this bias in a sequential foraging (prey selection) task and probe associated activation within the sympathetic branch of the autonomic system, using trial-by-trial measures of simultaneously recorded cardiac autonomic physiology. We reveal a unique adaptive role for the sympathetic branch in learning. It was specifically associated with adaptation to a deteriorating environment: it correlated with both the rate of negative information integration in belief estimates and downward changes in moment-to-moment environmental richness, and was predictive of optimal performance on the task. The findings are consistent with a framework whereby autonomic function supports the learning demands of prey selection.

Decision heuristics in contexts integrating action selection and execution.

Heuristics can inform human decision making in complex environments through a reduction of computational requirements (accuracy-resource trade-off) and a robustness to overparameterisation (less-is-more). However, tasks capturing the efficiency of heuristics typically ignore action proficiency in determining rewards. The requisite movement parameterisation in sensorimotor control questions whether heuristics preserve efficiency when actions are nontrivial. We developed a novel action selection-execution task requiring joint optimisation of action selection and spatio-temporal skillful execution. State-appropriate choices could be determined by a simple spatial heuristic, or by more complex planning. Computational models of action selection parsimoniously distinguished human participants who adopted the heuristic from those using a more complex planning strategy. Broader comparative analyses then revealed that participants using the heuristic showed combined decisional (selection) and skill (execution) advantages, consistent with a less-is-more framework. In addition, the skill advantage of the heuristic group was predominantly in the core spatial features that also shaped their decision policy, evidence that the dimensions of information guiding action selection might be yoked to salient features in skill learning.

Habituation of the stress response multiplex to repeated cold pressor exposure.

Humans show remarkable habituation to aversive events as reflected by changes of both subjective report and objective measures of stress. Although much experimental human research focuses on the effects of stress, relatively little is known about the cascade of physiological and neural responses that contribute to stress habituation. The cold pressor test (CPT) is a common method for inducing acute stress in human participants in the laboratory; however, there are gaps in our understanding of the global state changes resulting from this stress-induction technique and how these responses change over multiple exposures. Here, we measure the stress response to repeated CPT exposures using an extensive suite of physiologic measures and state-of-the-art analysis techniques. In two separate sessions on different days, participants underwent five 90 s CPT exposures of both feet and five warm water control exposures, while electrocardiography (ECG), impedance cardiography, continuous blood pressure, pupillometry, scalp electroencephalography (EEG), salivary cortisol and self-reported pain assessments were recorded. A diverse array of adaptive responses are reported that vary in their temporal dynamics within each exposure as well as habituation across repeated exposures. During cold-water exposure there was a cascade of changes across several cardiovascular measures (elevated heart rate (HR), cardiac output (CO) and Mean Arterial Pressure (MAP) and reduced left ventricular ejection time (LVET), stroke volume (SV) and high-frequency heart rate variability (HF)). Increased pupil dilation was observed, as was increased power in low-frequency bands (delta and theta) across frontal EEG electrode sites. Several cardiovascular measures also habituated over repeated cold-water exposures (HR, MAP, CO, SV, LVET) as did pupil dilation and alpha frequency activity across the scalp. Anticipation of cold water induced stress effects in the time-period immediately prior to exposure, indexed by increased pupil size and cortical disinhibition in the alpha and beta frequency bands across central scalp sites. These results provide comprehensive insight into the evolution of a diverse array of stress responses to an acute noxious stressor, and how these responses adaptively contribute to stress habituation.

Ventromedial Prefrontal Cortex Activity and Sympathetic Allostasis During Value-Based Ambivalence.

Anxiety is characterized by low confidence in daily decisions, coupled with high levels of phenomenological stress. Ventromedial prefrontal cortex (vmPFC) plays an integral role in maladaptive anxious behaviors via decreased sensitivity to threatening vs. non-threatening stimuli (fear generalization). vmPFC is also a key node in approach-avoidance decision making requiring two-dimensional integration of rewards and costs. More recently, vmPFC has been implicated as a key cortical input to the sympathetic branch of the autonomic nervous system. However, little is known about the role of this brain region in mediating rapid stress responses elicited by changes in confidence during decision making. We used an approach-avoidance task to examine the relationship between sympathetically mediated cardiac stress responses, vmPFC activity and choice behavior over long and short time-scales. To do this, we collected concurrent fMRI, EKG and impedance cardiography recordings of sympathetic drive while participants made approach-avoidance decisions about monetary rewards paired with painful electric shock stimuli. We observe first that increased sympathetic drive (shorter pre-ejection period) in states lasting minutes are associated with choices involving reduced decision ambivalence. Thus, on this slow time scale, sympathetic drive serves as a proxy for "mobilization" whereby participants are more likely to show consistent value-action mapping. In parallel, imaging analyses reveal that on shorter time scales (estimated with a trial-to-trial GLM), increased vmPFC activity, particularly during low-ambivalence decisions, is associated with decreased sympathetic state. Our findings support a role of sympathetic drive in resolving decision ambivalence across long time horizons and suggest a potential role of vmPFC in modulating this response on a moment-to-moment basis.

Quantifying rapid changes in cardiovascular state with a moving ensemble average.

MEAP, the moving ensemble analysis pipeline, is a new open-source tool designed to perform multisubject preprocessing and analysis of cardiovascular data, including electrocardiogram (ECG), impedance cardiogram (ICG), and continuous blood pressure (BP). In addition to traditional ensemble averaging, MEAP implements a moving ensemble averaging method that allows for the continuous estimation of indices related to cardiovascular state, including cardiac output, preejection period, heart rate variability, and total peripheral resistance, among others. Here, we define the moving ensemble technique mathematically, highlighting its differences from fixed-window ensemble averaging. We describe MEAP's interface and features for signal processing, artifact correction, and cardiovascular-based fMRI analysis. We demonstrate the accuracy of MEAP's novel B point detection algorithm on a large collection of hand-labeled ICG waveforms. As a proof of concept, two subjects completed a series of four physical and cognitive tasks (cold pressor, Valsalva maneuver, video game, random dot kinetogram) on 3 separate days while ECG, ICG, and BP were recorded. Critically, the moving ensemble method reliably captures the rapid cyclical cardiovascular changes related to the baroreflex during the Valsalva maneuver and the classic cold pressor response. Cardiovascular measures were seen to vary considerably within repetitions of the same cognitive task for each individual, suggesting that a carefully designed paradigm could be used to capture fast-acting event-related changes in cardiovascular state.