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Highlights
• Transcranial ultrasound neuromodulation/stimulation (TUS) is a growing field.
• We conducted a double-blind sham-controlled within-subjects large sample TUS study.
• Right prefrontal cortex TUS inhibits midfrontal theta electroencephalography (MFT).
• TUS MFT inhibition explains greater approach versus withdrawal in a virtual T-maze.
• This distinct TUS-MFT-behavior link merits future basic and applied research.
Abstract
Recent reviews highlighted low-intensity transcranial focused ultrasound (TUS) as a promising new tool for non-invasive neuromodulation in basic and applied sciences. Our preregistered double-blind within-subjects study (N = 152) utilized TUS targeting the right prefrontal cortex, which, in earlier work, was found to positively enhance self-reported global mood, decrease negative states of self-reported emotional conflict (anxiety/worrying), and modulate related midfrontal functional magnetic resonance imaging activity in affect regulation brain networks. To further explore TUS effects on objective physiological and behavioral variables, we used a virtual T-maze task that has been established in prior studies to measure motivational conflicts regarding whether participants execute approach versus withdrawal behavior (with free-choice responses via continuous joystick movements) while allowing to record related electroencephalographic data such as midfrontal theta activity (MFT). MFT, a reliable marker of conflict representation on a neuronal level, was of particular interest to us since it has repeatedly been shown to explain related behavior, with relatively low MFT typically preceding approach-like risky behavior and relatively high MFT typically preceding withdrawal-like risk aversion. Our central hypothesis is that TUS decreases MFT in T-maze conflict situations and thereby increases approach and reduces withdrawal. Results indicate that TUS led to significant MFT decreases, which significantly explained increases in approach behavior and decreases in withdrawal behavior. This study expands TUS evidence on a physiological and behavioral level with a large sample size of human subjects, suggesting the promise of further research based on this distinct TUS-MFT-behavior link to influence conflict monitoring and its behavioral consequences. Ultimately, this can serve as a foundation for future clinical work to establish TUS interventions for emotional and motivational mental health.
Approach and avoidance of positive and negative social cues are fundamental to prevent isolation and ensure survival. High trait social anxiety is characterized by an avoidance of social situations and extensive avoidance is a risk factor for the development of social anxiety disorder (SAD). Therefore, experimental methods to assess social avoidance behavior in humans are essential. The social conditioned place preference (SCPP) paradigm is a well-established experimental paradigm in animal research that is used to objectively investigate social approach–avoidance mechanisms. We retranslated this paradigm for human research using virtual reality. To this end, 58 healthy adults were exposed to either a happy- or angry-looking virtual agent in a specific room, and the effects of this encounter on dwell time as well as evaluation of this room in a later test without an agent were examined. We did not observe a general SCPP effect on dwell time or ratings but discovered a moderation by trait social anxiety, in which participants with higher trait social anxiety spent less time in the room in which the angry agent was present before, suggesting that higher levels of trait social anxiety foster conditioned social avoidance. However, further studies are needed to verify this observation and substantiate an association with social anxiety disorder. We discussed the strengths, limitations, and technical implications of our paradigm for future investigations to more comprehensively understand the mechanisms involved in social anxiety and facilitate the development of new personalized treatment approaches by using virtual reality.
Gazes are of central relevance for people. They are crucial for navigating the world and communicating with others. Nevertheless, research in recent years shows that many findings from experimental research on gaze behavior cannot be transferred from the laboratory to everyday behavior. For example, the frequency with which conspecifics are looked at is considerably higher in experimental contexts than what can be observed in daily behavior. In short: findings from laboratories cannot be generalized into general statements. This thesis is dedicated to this matter. The dissertation describes and documents the current state of research on social attention through a literature review, including a meta-analysis on the /gaze cueing/ paradigm and an empirical study on the robustness of gaze following behavior. In addition, virtual reality was used in one of the first studies in this research field. Virtual reality has the potential to significantly improve the transferability of experimental laboratory studies to everyday behavior. This is because the technology enables a high degree of experimental control in naturalistic research designs. As such, it has the potential to transform empirical research in the same way that the introduction of computers to psychological research did some 50 years ago. The general literature review on social attention is extended to the classic /gaze cueing/ paradigm through a systematic review of publications and a meta-analytic evaluation (Study 1). The cumulative evidence supported the findings of primary studies: Covert spatial attention is directed by faces. However, the experimental factors included do not explain the surprisingly large variance in the published results. Thus, there seem to be further, not well-understood variables influencing these social processes. Moreover, classic /gaze cueing/ studies have limited ecological validity. This is discussed as a central reason for the lack of generalisability. Ecological validity describes the correspondence between experimental factors and realistic situations. A stimulus or an experimental design can have high and low ecological validity on different dimensions and have different influences on behavior. Empirical research on gaze following behavior showed that the /gaze cueing/ effect also occurs with contextually embedded stimuli (Study 2). The contextual integration of the directional cue contrasted classical /gaze cueing/ studies, which usually show heads in isolation. The research results can thus be transferred /within/ laboratory studies to higher ecologically valid research paradigms. However, research shows that the lack of ecological validity in experimental designs significantly limits the transferability of experimental findings to complex situations /outside/ the laboratory. This seems to be particularly the case when social interactions and norms are investigated. However, ecological validity is also often limited in these studies for other factors, such as contextual embedding /of participants/, free exploration behavior (and, thus, attentional control), or multimodality. In a first study, such high ecological validity was achieved for these factors with virtual reality, which could not be achieved in the laboratory so far (Study 3). Notably, the observed fixation patterns showed differences even under /most similar/ conditions in the laboratory and natural environments. Interestingly, these were similar to findings also derived from comparisons of eye movement in the laboratory and field investigations. These findings, which previously came from hardly comparable groups, were thus confirmed by the present Study 3 (which did not have this limitation). Overall, /virtual reality/ is a new technical approach to contemporary social attention research that pushes the boundaries of previous experimental research. The traditional trade-off between ecological validity and experimental control thus becomes obsolete, and laboratory studies can closely inherit an excellent approximation of reality. Finally, the present work describes and discusses the possibilities of this technology and its practical implementation. Within this context, the extent to which this development can still guarantee a constructive classification of different laboratory tests in the future is examined.
Effects of Acrophobic Fear and Trait Anxiety on Human Behavior in a Virtual Elevated Plus-Maze
(2021)
The Elevated Plus-Maze (EPM) is a well-established apparatus to measure anxiety in rodents, i.e., animals exhibiting an increased relative time spent in the closed vs. the open arms are considered anxious. To examine whether such anxiety-modulated behaviors are conserved in humans, we re-translated this paradigm to a human setting using virtual reality in a Cave Automatic Virtual Environment (CAVE) system. In two studies, we examined whether the EPM exploration behavior of humans is modulated by their trait anxiety and also assessed the individuals’ levels of acrophobia (fear of height), claustrophobia (fear of confined spaces), sensation seeking, and the reported anxiety when on the maze. First, we constructed an exact virtual copy of the animal EPM adjusted to human proportions. In analogy to animal EPM studies, participants (N = 30) freely explored the EPM for 5 min. In the second study (N = 61), we redesigned the EPM to make it more human-adapted and to differentiate influences of trait anxiety and acrophobia by introducing various floor textures and lower walls of closed arms to the height of standard handrails. In the first experiment, hierarchical regression analyses of exploration behavior revealed the expected association between open arm avoidance and Trait Anxiety, an even stronger association with acrophobic fear. In the second study, results revealed that acrophobia was associated with avoidance of open arms with mesh-floor texture, whereas for trait anxiety, claustrophobia, and sensation seeking, no effect was detected. Also, subjects’ fear rating was moderated by all psychometrics but trait anxiety. In sum, both studies consistently indicate that humans show no general open arm avoidance analogous to rodents and that human EPM behavior is modulated strongest by acrophobic fear, whereas trait anxiety plays a subordinate role. Thus, we conclude that the criteria for cross-species validity are met insufficiently in this case. Despite the exploratory nature, our studies provide in-depth insights into human exploration behavior on the virtual EPM.
Background: The rehabilitation of gait disorders in patients with multiple sclerosis (MS) and stroke is often based on conventional treadmill training. Virtual reality (VR)-based treadmill training can increase motivation and improve therapy outcomes. The present study evaluated an immersive virtual reality application (using a head-mounted display, HMD) for gait rehabilitation with patients to (1) demonstrate its feasibility and acceptance and to (2) compare its short-term effects to a semi-immersive presentation (using a monitor) and a conventional treadmill training without VR to assess the usability of both systems and estimate the effects on walking speed and motivation. Methods: In a within-subjects study design, 36 healthy participants and 14 persons with MS or stroke participated in each of the three experimental conditions (VR via HMD, VR via monitor, treadmill training without VR). Results: For both groups, the walking speed in the HMD condition was higher than in treadmill training without VR and in the monitor condition. Healthy participants reported a higher motivation after the HMD condition as compared with the other conditions. Importantly, no side effects in the sense of simulator sickness occurred and usability ratings were high. No increases in heart rate were observed following the VR conditions. Presence ratings were higher for the HMD condition compared with the monitor condition for both user groups. Most of the healthy study participants (89%) and patients (71%) preferred the HMD-based training among the three conditions and most patients could imagine using it more frequently. Conclusions For the first time, the present study evaluated the usability of an immersive VR system for gait rehabilitation in a direct comparison with a semi-immersive system and a conventional training without VR with healthy participants and patients. The study demonstrated the feasibility of combining a treadmill training with immersive VR. Due to its high usability and low side effects, it might be particularly suited for patients to improve training motivation and training outcome e. g. the walking speed compared with treadmill training using no or only semi-immersive VR. Immersive VR systems still require specific technical setup procedures. This should be taken into account for specific clinical use-cases during a cost-benefit assessment.
Animals, just like humans, can freely move. They do so for various important reasons, such as finding food and escaping predators. Observing these behaviors can inform us about the underlying cognitive processes. In addition, while humans can convey complicated information easily through speaking, animals need to move their bodies to communicate. This has prompted many creative solutions by animal neuroscientists to enable studying the brain during movement. In this review, we first summarize how animal researchers record from the brain while an animal is moving, by describing the most common neural recording techniques in animals and how they were adapted to record during movement. We further discuss the challenge of controlling or monitoring sensory input during free movement.
However, not only is free movement a necessity to reflect the outcome of certain internal cognitive processes in animals, it is also a fascinating field of research since certain crucial behavioral patterns can only be observed and studied during free movement. Therefore, in a second part of the review, we focus on some key findings in animal research that specifically address the interaction between free movement and brain activity. First, focusing on walking as a fundamental form of free movement, we discuss how important such intentional movements are for understanding processes as diverse as spatial navigation, active sensing, and complex motor planning. Second, we propose the idea of regarding free movement as the expression of a behavioral state. This view can help to understand the general influence of movement on brain function.
Together, the technological advancements towards recording from the brain during movement, and the scientific questions asked about the brain engaged in movement, make animal research highly valuable to research into the human “moving brain”.
Stronger reactivity to social gaze in virtual reality compared to a classical laboratory environment
(2021)
People show a robust tendency to gaze at other human beings when viewing images or videos, but were also found to relatively avoid gaze at others in several real‐world situations. This discrepancy, along with theoretical considerations, spawned doubts about the appropriateness of classical laboratory‐based experimental paradigms in social attention research. Several researchers instead suggested the use of immersive virtual scenarios in eliciting and measuring naturalistic attentional patterns, but the field, struggling with methodological challenges, still needs to establish the advantages of this approach. Here, we show using eye‐tracking in a complex social scenario displayed in virtual reality that participants show enhanced attention towards the face of an avatar at near distance and demonstrate an increased reactivity towards her social gaze as compared to participants who viewed the same scene on a computer monitor. The present study suggests that reactive virtual agents observed in immersive virtual reality can elicit natural modes of information processing and can help to conduct ecologically more valid experiments while maintaining high experimental control.
Pointing is a ubiquitous means of communication. Nevertheless, observers systematically misinterpret the location indicated by pointers. We examined whether these misunderstandings result from the typically different viewpoints of pointers and observers. Participants either pointed themselves or interpreted points while assuming the pointer’s or a typical observer perspective in a virtual reality environment. The perspective had a strong effect on the relationship between pointing gestures and referents, whereas the task had only a minor influence. This suggests that misunderstandings between pointers and observers primarily result from their typically different viewpoints.
Acrophobia is characterized by intense fear in height situations. Virtual reality (VR) can be used to trigger such phobic fear, and VR exposure therapy (VRET) has proven effective for treatment of phobias, although it remains important to further elucidate factors that modulate and mediate the fear responses triggered in VR. The present study assessed verbal and behavioral fear responses triggered by a height simulation in a 5-sided cave automatic virtual environment (CAVE) with visual and acoustic simulation and further investigated how fear responses are modulated by immersion, i.e., an additional wind simulation, and presence, i.e., the feeling to be present in the VE. Results revealed a high validity for the CAVE and VE in provoking height related self-reported fear and avoidance behavior in accordance with a trait measure of acrophobic fear. Increasing immersion significantly increased fear responses in high height anxious (HHA) participants, but did not affect presence. Nevertheless, presence was found to be an important predictor of fear responses. We conclude that a CAVE system can be used to elicit valid fear responses, which might be further enhanced by immersion manipulations independent from presence. These results may help to improve VRET efficacy and its transfer to real situations.
This thesis aims for a better understanding of the mechanisms underlying anxiety as well as trauma- and stressor-related disorders and the development of new therapeutic approaches. I was first interested in the associative learning mechanisms involved in the etiology of anxiety disorders. Second, I explored the therapeutic effects of transcutaneous vagus nerve stimulation (tVNS) as a promising new method to accelerate and stabilize extinction learning in humans.
For these purposes, I applied differential anxiety conditioning protocols realized by the implementation of virtual reality (VR). Here, a formerly neutral virtual context (anxiety context, CTX+) is presented whereby the participants unpredictably receive mildly aversive electric stimuli (unconditioned stimulus, US). Another virtual context (safety context, CTX-) is never associated with the US. Moreover, extinction of conditioned anxiety can be modeled by presenting the same contexts without US delivery. When unannounced USs were administered after extinction, i.e. reinstatement, the strength of the “returned” conditioned anxiety can provide information on the stability of the extinction memory.
In Study 1, I disentangled the role of elemental and conjunctive context representations in the acquisition of conditioned anxiety. Sequential screenshots of two virtual offices were presented like a flip-book so that I elicited the impression of walking through the contexts. Some pictures of CTX+ were paired with an US (threat elements), but not some other screenshots of the same context (non-threat elements), nor the screenshots depicting CTX- (safety elements). Higher contingency ratings for threat compared to non-threat elements revealed elemental representation. Electro-cortical responses showed larger P100 and early posterior negativity amplitudes elicited by screenshots depicting CTX+ compared to CTX- and suggested conjunctive representation. These results support the dual context representation in anxiety acquisition in healthy individuals.
Study 2 addressed the effects of tVNS on the stabilization of extinction learning by using a context conditioning paradigm. Potentiated startle responses as well as higher aversive ratings in CTX+ compared to CTX- indicate successful anxiety conditioning. Complete extinction was found in startle responses and valence ratings as no differentiation between CTX+ and CTX- suggested. TVNS did not affect extinction or reinstatement of anxiety which may be related to the inappropriate transferability of successful stimulation parameters from epilepsy patients to healthy participants during anxiety extinction.
Therefore, in Study 3 I wanted to replicate the modulatory effects of tVNS on heart rate and pain perception by the previously used parameters. However, no effects of tVNS were observed on subjective pain ratings, on pain tolerance, or on heart rate. This led to the conclusion that the modification of stimulation parameters is necessary for a successful acceleration of anxiety extinction in humans.
In Study 4, I prolonged the tVNS and, considering previous tVNS studies, I applied a cue conditioning paradigm in VR. Therefore, during acquisition a cue (CS+) presented in CTX+ predicted the US, but not another cue (CS-). Both cues were presented in a second context (CTX-) and never paired with the US. Afterward, participants received either tVNS or sham stimulation and underwent extinction learning. I found context-dependent cue conditioning only in valence ratings, which was indicated by lower valence for CS+ compared to CS- in CTX+, but no differential ratings in CTX-. Successful extinction was indicated by equal responses to CS+ and CS-. Interestingly, I found reinstatement of conditioned fear in a context-dependent manner, meaning startle response was potentiated for CS+ compared to CS- only in the anxiety context. Importantly, even the prolonged tVNS had no effect, neither on extinction nor on reinstatement of context-dependent cue conditioning. However, I found first evidence for accelerated physiological contextual extinction due to less differentiation between startles in CTX+ compared to CTX- in the tVNS than in the sham stimulated group.
In sum, this thesis first confirms the dual representation of a context in an elemental and a conjunctive manner. Second, though anxiety conditioning and context-dependent cue conditioning paradigms worked well, the translation of tVNS accelerated extinction from rats to humans needs to be further developed, especially the stimulation parameters. Nevertheless, tVNS remains a very promising approach of memory enhancement, which can be particularly auspicious in clinical settings.