Independent replications reveal anterior and posterior cingulate cortex activation underlying state anxiety-attenuated face encoding.

Anxiety involves the anticipation of aversive outcomes and can impair neurocognitive processes, such as the ability to recall faces encoded during the anxious state. It is important to precisely delineate and determine the replicability of these effects using causal state anxiety inductions in the general population. This study therefore aimed to replicate prior research on the distinct impacts of threat-of-shock-induced anxiety on the encoding and recognition stage of emotional face processing, in a large asymptomatic sample (n = 92). We successfully replicated previous results demonstrating impaired recognition of faces encoded under threat-of-shock. This was supported by a mega-analysis across three independent studies using the same paradigm (n = 211). Underlying this, a whole-brain fMRI analysis revealed enhanced activation in the posterior cingulate cortex (PCC), alongside previously seen activity in the anterior cingulate cortex (ACC) when combined in a mega-analysis with the fMRI findings we aimed to replicate. We further found replications of hippocampus activation when the retrieval and encoding states were congruent. Our results support the notion that state anxiety disrupts face recognition, potentially due to attentional demands of anxious arousal competing with affective stimuli processing during encoding and suggest that regions of the cingulate cortex play pivotal roles in this.

Anxiety Shapes Amygdala-Prefrontal Dynamics During Movie Watching.

Background: A well-characterized amygdala-dorsomedial prefrontal circuit is thought to be crucial for threat vigilance during anxiety. However, engagement of this circuitry within relatively naturalistic paradigms remains unresolved. Methods: Using an open functional magnetic resonance imaging dataset (Cambridge Centre for Ageing Neuroscience; n = 630), we sought to investigate whether anxiety correlates with dynamic connectivity between the amygdala and dorsomedial prefrontal cortex during movie watching. Results: Using an intersubject representational similarity approach, we saw no effect of anxiety when comparing pairwise similarities of dynamic connectivity across the entire movie. However, preregistered analyses demonstrated a relationship between anxiety, amygdala-prefrontal dynamics, and anxiogenic features of the movie (canonical suspense ratings). Our results indicated that amygdala-prefrontal circuitry was modulated by suspense in low-anxiety individuals but was less sensitive to suspense in high-anxiety individuals. We suggest that this could also be related to slowed habituation or amplified anticipation. Moreover, a measure of threat-relevant attentional bias (accuracy/reaction time to fearful faces) demonstrated an association with connectivity and suspense. Conclusions: Overall, this study demonstrated the presence of anxiety-relevant differences in connectivity during movie watching, varying with anxiogenic features of the movie. Mechanistically, exactly how and when these differences arise remains an opportunity for future research.

Threat vigilance and intrinsic amygdala connectivity.

A well-documented amygdala-dorsomedial prefrontal circuit is theorized to promote attention to threat ("threat vigilance"). Prior research has implicated a relationship between individual differences in trait anxiety/vigilance, engagement of this circuitry, and anxiogenic features of the environment (e.g., through threat-of-shock and movie-watching). In the present study, we predicted that-for those scoring high in self-reported anxiety and a behavioral measure of threat vigilance-this circuitry is chronically engaged, even in the absence of anxiogenic stimuli. Our analyses of resting-state fMRI data (N = 639) did not, however, provide evidence for such a relationship. Nevertheless, in our planned exploratory analyses, we saw a relationship between threat vigilance behavior (but not self-reported anxiety) and intrinsic amygdala-periaqueductal gray connectivity. Here, we suggest this subcortical circuitry may be chronically engaged in hypervigilant individuals, but that amygdala-prefrontal circuitry may only be engaged in response to anxiogenic stimuli.

RapidHRV: an open-source toolbox for extracting heart rate and heart rate variability.

Heart rate and heart rate variability have enabled insight into a myriad of psychophysiological phenomena. There is now an influx of research attempting using these metrics within both laboratory settings (typically derived through electrocardiography or pulse oximetry) and ecologically-rich contexts (via wearable photoplethysmography, i.e., smartwatches). However, these signals can be prone to artifacts and a low signal to noise ratio, which traditionally are detected and removed through visual inspection. Here, we developed an open-source Python package, RapidHRV, dedicated to the preprocessing, analysis, and visualization of heart rate and heart rate variability. Each of these modules can be executed with one line of code and includes automated cleaning. In simulated data, RapidHRV demonstrated excellent recovery of heart rate across most levels of noise (>=10 dB) and moderate-to-excellent recovery of heart rate variability even at relatively low signal to noise ratios (>=20 dB) and sampling rates (>=20 Hz). Validation in real datasets shows good-to-excellent recovery of heart rate and heart rate variability in electrocardiography and finger photoplethysmography recordings. Validation in wrist photoplethysmography demonstrated RapidHRV estimations were sensitive to heart rate and its variability under low motion conditions, but estimates were less stable under higher movement settings.

Anxiety and amygdala connectivity during movie-watching.

Rodent and human studies have implicated an amygdala-prefrontal circuit during threat processing. One possibility is that while amygdala activity underlies core features of anxiety (e.g. detection of salient information), prefrontal cortices (i.e. dorsomedial prefrontal/anterior cingulate cortex) entrain its responsiveness. To date, this has been established in tightly controlled paradigms (predominantly using static face perception tasks) but has not been extended to more naturalistic settings. Consequently, using 'movie fMRI'-in which participants watch ecologically-rich movie stimuli rather than constrained cognitive tasks-we sought to test whether individual differences in anxiety correlate with the degree of face-dependent amygdala-prefrontal coupling in two independent samples. Analyses suggested increased face-dependent superior parietal activation and decreased speech-dependent auditory cortex activation as a function of anxiety. However, we failed to find evidence for anxiety-dependent connectivity, neither in our stimulus-dependent or -independent analyses. Our findings suggest that work using experimentally constrained tasks may not replicate in more ecologically valid settings and, moreover, highlight the importance of testing the generalizability of neuroimaging findings outside of the original context.

Titrating the Smell of Fear: Initial Evidence for Dose-Invariant Behavioral, Physiological, and Neural Responses.

It is well accepted that emotional intensity scales with stimulus strength. Here, we used physiological and neuroimaging techniques to ask whether human body odor-which can convey salient social information-also induces dose-dependent effects on behavior, physiology, and neural responses. To test this, we first collected sweat from 36 males classified as low-, medium-, and high-fear responders. Next, in a double-blind within-subjects functional-MRI design, 31 women were exposed to three doses of fear-associated human chemosignals and neutral sweat while viewing face morphs varying between expressions of fear and disgust. Behaviorally, we found that all doses of fear-sweat volatiles biased participants toward perceiving fear in ambiguous morphs, a dose-invariant effect generally repeated across physiological and neural measures. Bayesian dose-response analysis indicated moderate evidence for the null hypothesis (except for the left amygdala), tentatively suggesting that the human olfactory system engages an all-or-none mechanism for tagging fear above a minimal threshold.

Trait anxiety does not correlate with metacognitive confidence or reminder usage in a delayed intentions task.

Setting external reminders provides a convenient way to reduce cognitive demand and ensure accurate retrieval of information for prospective tasks. Recent experimental evidence has demonstrated that the decision to offload cognitive information to external resources is guided by metacognitive belief, that is, individuals' confidence in their unaided ability. Other work has also suggested a relationship between metacognitive belief and trait anxiety. In the present study (N = 300), we bridged these two areas by investigating whether trait anxiety correlated with metacognitive belief and-consequently-propensity to offload information in a delayed intentions paradigm. Participants received a financial reward based on their ability to remember targets. However, participants could take a reduced reward per target if they decided to use reminders. We replicated previous findings that participants were biased to use more reminders than would be optimal, and this bias was correlated with metacognitive judgements. However, we show no evidence that trait anxiety held a relationship with metacognitive belief or reminder usage. Indeed, Bayesian analyses strongly favoured the null. Therefore, variation in self-reported trait anxiety does not necessarily influence confidence and strategy when participants remember delayed intentions.

Does overloading cognitive resources mimic the impact of anxiety on temporal cognition?

Anxiety alters how we perceive the world and can alter aspects of cognitive performance. Prominent theories of anxiety suggest that the effect of anxiety on cognition is due to anxious thoughts "overloading" limited cognitive resources, competing with other processes. If this is so, then a cognitive load manipulation should impact performance of a task in the same way as induced anxiety. Thus, we examined the impact of a load manipulation on a time perception task that we have previously shown to be reliably impacted by anxiety. In contrast with our prediction, across 3 studies we found that time perception was insensitive to our load manipulation. Our results do not therefore support the idea that anxiety impacts temporal cognition by overloading limited cognitive resources, at least as induced by a commonly used load manipulation. Thus, anxiety might affect temporal cognition in a unique way, via an evolutionary-preserved defense survival system, as suggested by animal-inspired theories of anxiety, rather than competing for limited attentional resources. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Encoding fear intensity in human sweat.

Humans, like other animals, have an excellent sense of smell that can serve social communication. Although ample research has shown that body odours can convey transient emotions like fear, these studies have exclusively treated emotions as categorical, neglecting the question whether emotion quantity can be expressed chemically. Using a unique combination of methods and techniques, we explored a dose-response function: Can experienced fear intensity be encoded in fear sweat? Specifically, fear experience was quantified using multivariate pattern classification (combining physiological data and subjective feelings with partial least-squares-discriminant analysis), whereas a photo-ionization detector quantified volatile molecules in sweat. Thirty-six male participants donated sweat while watching scary film clips and control (calming) film clips. Both traditional univariate and novel multivariate analysis (100% classification accuracy; Q2: 0.76; R2: 0.79) underlined effective fear induction. Using their regression-weighted scores, participants were assigned significantly above chance (83% > 33%) to fear intensity categories (low-medium-high). Notably, the high fear group (n = 12) produced higher doses of armpit sweat, and greater doses of fear sweat emitted more volatile molecules (n = 3). This study brings new evidence to show that fear intensity is encoded in sweat (dose-response function), opening a field that examines intensity coding and decoding of other chemically communicable states/traits. This article is part of the Theo Murphy meeting issue 'Olfactory communication in humans'.