Ann. N.Y. Acad. Sci. ISSN 0077-8923

A N N A L S O F T H E N E W Y O R K A C A D E M Y O F SC I E N C E S Issue: Dizziness and Balance Disorders

Acrophobia impairs visual exploration and balance during standing and walking Thomas Brandt,1 Gunter Kugler,1 Roman Schniepp,1,2 Max Wuehr,1 and Doreen Huppert1 ¨ 1 2

German Center for Vertigo and Balance Disorders, Ludwig-Maximilians-University of Munich, Munich, Germany. Department of Neurology, Ludwig-Maximilians-University of Munich, Munich, Germany

Address for correspondence: Thomas Brandt, M.D., F.R.C.P., F.A.N.A., German Center for Vertigo and Balance Disorders, Ludwig-Maximilians-University of Munich, Marchioninistr. 15, 81377 Munich, Germany. [email protected]

This review shows that persons with visual height intolerance or acrophobia exhibit typical restrictions of visual exploration and imbalance during stance and locomotion when exposed to heights. Eye and head movements are reduced, and gaze freezes to the horizon. Eye movements tend to be horizontal saccades during stance and vertical saccades during locomotion. Body posture is characterized by a stiffening of the musculoskeletal system with increased open-loop diffusion activity of body sway, a lowered sensory feedback threshold for closed-loop balance control, and increased co-contraction of antigravity leg and neck muscles. Walking is slow and cautious, broad-based, consisting of small, flat-footed steps with less dynamic vertical oscillation of the body and head. Anxiety appears to be the critical symptom that causes the typical but not specific eye and body motor behavior, which can be described as tonic immobility. Guidelines for preventing acrophobia, which could be an add-on to behavioral therapy, are provided. Keywords: acrophobia; fear of heights; visual height intolerance; visual exploration; stance; gait

Anxiety and visual height intolerance Recent population-based cross-sectional epidemiological studies confirmed that the most prominent symptom of visual height intolerance is fearfulness1 and that visual height intolerance and even more so acrophobia are associated with high rates of comorbid anxious and depressive conditions.2 The lifetime prevalence of visual height intolerance is 28% (females 32%; males 25%) of the general population;1 in more than 20% of those afflicted it occasionally develops into panic attacks.2 The lifetime prevalence of its more severe variant acrophobia or fear of heights––a specific phobia according to the Diagnostic and Statistical Manual of Mental Disorders (DSM-V)––ranges from 3.1% to 6.4%.2–4 As a rule, acrophobia requires psychotherapy. The following three terms have been proposed in order to distinguish three quite different reactions to heights. Their adoption may resolve some confusion about the physiological and psychopathological mechanisms active during exposure to visual heights.5,6 The yardstick for clinical relevance was the complaint of susceptible persons that the

distressing condition restricts daily life activities and causes them to avoid precipitating stimuli. 1. A physiological height imbalance, caused by impaired visual control of postural balance with a prevalence of 100%, but of no clinical relevance. 2. Visual height intolerance, which manifests as more or less distress and anxiety when exposed to heights with a prevalence of 28% and a clinical relevance of 50% of those afflicted. 3. Acrophobia or fear of heights, a specific phobia according to DSM-V with a prevalence of 3.1–6.4% and a clinical relevance of 100%. Psychotherapy is recommended, if susceptible individuals cannot satisfactorily cope with the feared stimuli. In their historical review of the medical literature since antiquity, Balaban and Jacob7 present a fascinating overview of the comorbidity of anxiety and vertigo as an integral condition. Plato used the same terms to describe vertigo, inebriation, height

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vertigo, disorientation, and mental confusion.7 Vivid images of fear of heights can be found in Greek, Roman, and Chinese classics, such as the Greek Corpus Hippocraticum, from the 5th century BC, texts from Ovid on Roman mythology,8 or in the Chinese book Huangdi Neijing Lingshu,9 the international classic of the Yellow Thearch, which serves as the theoretical foundation of Chinese medicine. In the 18th century, Johann Wolfgang von Goethe entertained his literary circle in Strasbourg with reports of how he had cured his “fear of heights” (hoehenangst) by repeatedly climbing the tower of the Strasbourg Cathedral,10 a method called flooding in current behavioral therapy. For Sigmund Freud,11 fear of heights was a form of anxiety neurosis (angstneurose). The term acrophobia dates back to the late 19th century12 and is derived from the Greek words akros, meaning peak, summit, edge, and phobia, fear. The Italian psychiatrist Andrea Verga first used it to describe his own experience of exaggerated fear when being in high places. The historical tendency to interpret fear of heights purely psychopathologically might be responsible for the relatively scarce experimental neurophysiological studies on the phenomenon. Erasmus Darwin, in his Zoonomia or the Laws of Organic Life in 1794, was possibly the first to hypothesize that nonpsychological sensorimotor mechanisms cause postural imbalance at heights.13 In the following, we will discuss how visual exposure to heights affects eye movements, visual exploration, and balance during stance and locomotion. We will focus on the question of whether acrophobia and visual height intolerance elicit typical patterns of eye and body movements, and whether these patterns are specific or unspecific motor reactions to anxiety. Eye movements and visual exploration in specific phobias The influence of various types of anxiety (e.g., state anxiety, trait anxiety, and psychiatric anxiety disorders) on ocular motor control and gaze has been well acknowledged.14 Its importance is especially evident in eye movement recordings in patients with animal and social phobias. The avoidance of the threatening stimulus15 is a common feature of all phobias. One would expect gaze behavior to be different in the case of specific animal phobias. Subjects with animal phobias like spider phobia or snake phobia are generally thought to fixate the animals continually 38

in order to maintain control of the situation and to react early if the feared animals come any closer. However, this is not the case. When exposed to a picture of a spider and a picture of a flower, individuals who fear spiders look significantly more at the spiders in the initial presentation phase of the stimulus, but subsequently shift their view more often away from the spiders.16 This finding was confirmed by others.17,18 Their term hypervigilance-avoidance pattern describes such behavior in phobic individuals, compared to control individuals. The phobics detect spiders faster and fixate them longer during the initial search phase, but subsequently fixate them less. In another experiment, spider phobic individuals showed accelerated reflexive saccades in one of the basic ocular-motor tasks, whereas the fearrelevant exploration task evoked a general slowing of their scanning behavior and a pronounced ocular-motor avoidance.19 A similar attentional bias was found in subjects with an injection phobia.20 A hypervigilance-avoidance pattern was also found in individuals with social phobias21 and anxiety in general,22,23 and even in nonhuman primates, such as rhesus macaques.24 Cisler and Koster25 presented evidence showing how the mechanisms of attentional biases of threat and anxiety disorders function. A threat-detection mechanism facilitates attention, an attentional-control ability promotes disengagement, and attentional avoidance helps regulate emotional responses. Facilitated attention is explained to be an automatic reflex; emotion regulation, a strategy; and difficulty in disengagement, a mixture of automatic and strategic processing. Facilitated attention is anatomically attributed to neural circuits around the amygdala; the other two processes, to prefrontal cortex circuits.25 How acrophobia restricts eye movements and gaze in space during stance and locomotion Gaze behavior of individuals susceptible to visual height intolerance and acrophobia when exposed to heights has not been studied until very recently.26,27 These experiments did not examine the temporal aspect of exploratory behavior as regards an initial attentional bias toward the depth. The data were mainly concerned with how views of depth were avoided and how attention was self-focused on particular structures in the environment.

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Scene Camera

Binocular Cameras

Infrared Mirrors

Head Extension

45° 45°

15 meters above ground-level Semispinalis Capitis

Triceps Brachii

Head Upright

Sternocleidomastoid Head Flexion Biceps Brachii

Mobile EMG Device

Protective Railing

Tibialis Anterior Soleus Force Plate

Figure 1. Individuals with visual height intolerance and controls were exposed to height on an escape balcony about 15 m above ground level. They were asked to look from the balcony while standing upright or walking along the balcony (left panel). Eye and head movements were simultaneously recorded by a head-fixed goggle system (right panel, top). This included binocular infrared cameras for measuring eye movements, a head-fixed scene camera, and 6-degrees-of-freedom inertial sensors for detecting head movements in the yaw, pitch, and roll planes. For measurements of postural sway and antigravity muscle activity, participants stood on a force plate, with which center-of-pressure displacements were assessed. Electromyographic data of three muscle pairs were recorded with a mobile EMG device fixed around the waist and with electrodes on the tibialis anterior and soleus muscles of the leg, biceps brachii and triceps brachii of the arm, and sternocleidomastoid and semispinalis capitis of the neck. The stance protocol included various conditions indicated in the schematic drawing (right panel, bottom). Modified after Refs. 26 and 29.

Spontaneous movements of eyes and head were recorded both separately and simultaneously in individuals susceptible to fear of heights and in controls while standing still on an emergency balcony26 or while walking on the balcony.27 The balcony had a metallic floor grid and was equipped with a hand rail that provided safety while ensuring an unrestricted field of view and the exposure to heights (Fig. 1). Participants wore mobile infrared eye-tracking goggles with a head-fixed scene camera and integrated 6-degrees-of-freedom inertial sensors for recording head movements. During stance, susceptible individuals exhibited fewer and smaller-amplitude eye-in-head saccades with

fixations of longer duration. During locomotion, their total eye movements (saccade amplitudes, frequencies, fixation durations) did not differ from those of control individuals. However, there was a typical anisotropy for eye movements, especially in susceptible individuals. They exhibited a preference for the horizontal direction of saccades during stance and a preference for the vertical direction of saccades during locomotion (Fig. 2, top). Spontaneous head movements were reduced in susceptible individuals. The mean absolute angular velocity was significantly lower in all three planes (yaw, pitch, and roll) in both conditions (standing and walking). The range of head orientations of

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Saccade Histogram Upright Stance

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Figure 2. Spontaneous visual exploration of the surroundings by saccadic eye movements and head movements in the horizontal (yaw) plane and the vertical (pitch) plane during upright stance when exposed to heights on a balcony (see Fig. 1). Histograms of saccadic eye movements (top row) according to their direction in subjects with visual height intolerance (red) and controls (blue) during upright stance (left) as compared to locomotion (right). Dotted circles indicate percentage of eye movements performed in angular ranges of 6°. During upright stance, individuals susceptible to visual height intolerance exhibit preferably horizontal saccadic eye movements along the horizon. During locomotion, there is a different anisotropy: saccades are mainly made in the vertical direction. Group means of median head orientation (crosses) and interquartile ranges (bars) are depicted (bottom row). Susceptible individuals show significantly fewer head movements, particularly in the vertical pitch plane, when standing (bottom left). During locomotion, they keep their heads stiffly straight ahead in the direction of locomotion and avoid rotations toward the open side of the balcony (bottom right). Modified after Refs. 26 and 27.

susceptible individuals, while standing or walking on the balcony, was restricted in the horizontal (yaw) and vertical planes (pitch; Fig. 2, bottom). This was more pronounced in the pitch direction during stance. During locomotion, susceptible individuals directed their heads less often towards the open side of the balcony, but kept them relatively stiff in a straight-ahead direction. Reference points were tracked in the video frames of the head-fixed camera to determine head orientation, defined as a horizontal and vertical rotation (head torsion in roll plane was ignored). To determine gaze-in-space, head and gaze orientations were combined. To approximate the extent of the explored surroundings, we attributed

40

a solid angle to each fixation made. The assigned angle for each fixation equaled the solid angle of a cone with an apex angle roughly corresponding to the size of the fovea. The total solid angle covered, that is, the overlay of all fixations during exploration, is presented in a Mollweide equal area projection.26 Susceptible individuals exhibited a restricted exploratory behavior compared to that of control individuals (Fig. 3), and this correlated significantly with the severity of the perceived fear of heights. During upright stance, susceptible individuals showed two major eye and head movement strategies. One strategy was to fixate and explore the horizon, another was to freeze gaze to a small area straight ahead on the horizon or somewhat

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Acrophobia impairs exploration, stance, and gait

Figure 3. Gaze in space, for example, fixations of environmental structures, can be calculated from eye-in-head and head movements. The figure shows the distribution of fixations in space during approximately 30 s of upright stance (left) and approximately 15 s of locomotion (right) on the balcony. The time controls (top row) and susceptible individuals (bottom row) spent exploring the corresponding environmental structures are shown in Mollweide equal area projection for both, upright stance and locomotion, conditions. Susceptible individuals exhibit a restricted exploratory behavior compared to that of controls, with a preferred fixation along the horizon during upright stance (left). During locomotion (right), susceptible individuals avoid exploring the open side of the balcony and maintain their fixation mostly straight ahead and downward to the floor of the balcony. Modified after Refs. 26 and 27.

below. During locomotion, susceptible individuals avoided looking toward the open side of the balcony, but maintained their fixation straight ahead, covering an area vertically from the horizon to the ground in front of their feet (Fig. 3, bottom right). Avoiding looking into the abyss, but instead fixating the horizon, can be interpreted as an attempt to alleviate anxiety, because the horizontal distance to remote visual targets is not as threatening as depth is. This is in line with the general tendency of susceptible individuals to avoid situations involving exposure to heights.1,28 The preferred gaze-in-space (horizontal during stance and vertical during locomotion) is task

dependent. It is essential for navigation and balance control during locomotion. Visual control of locomotion has two requirements: the heading direction must be determined30,31 and stationary contrasts within the visual field must be present for postural stability,27,32 especially for lateral stabilization of gait.33 Eyes, head, and body are always directed toward the intended path.34 In addition, an individual’s gaze must be two steps ahead of foot placement in order to avoid obstacles when traversing a complex terrain.35 A limited gaze behavior thus increases the risk of falling during locomotion. In view of the above-mentioned findings on how eye movements and locomotion affect the anxiety

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of susceptible individuals at heights, behavioral therapy needs to devise strategies to take this into consideration.6,29 Physiological postural imbalance at heights due to impaired visual detection of body sway There is a simple geometrical explanation for physiological height imbalance. It occurs when the distance between the individual’s eyes and the nearest visible stationary contrasts in the surroundings becomes critically large.32,35 To maintain upright postural stability, afferent signals must be generated as an input for motor compensation of natural fore– aft and lateral body sway. This requires continuous central evaluation of the re-afferent sensory signals of self-generated body movements. Vision plays a major role in postural stabilization. Lateral head or body sway, for example, causes either a shift of the visual surround on the retina when the eyes are stationary in the head or eye movements with an angle corresponding to the shift if the object is fixated. This involves afferent or efferent motion perception (either by a re-afference or efference copy signal of the eye movements), respectively. In fact, it has been shown experimentally that the suppression of spontaneous nystagmus in vestibular disorders improves balance37 and that voluntary slow eye movements increase body sway.38 Body sway must increase for both types of perception of head motion with increasing distance to the nearest contrasts, because angular displacement of the environment on the retina becomes smaller (Fig. 4). Because an angular displacement on the retina of the visual scene of 20 min of arc is necessary to be detected by the paracentral and peripheral parts of the retina,39,40 a normal lateral head sway of 2 cm would be subthreshold at a distance of about 3 m.32,36 Below this threshold, there is a perceptional conflict, because the vestibular and somatosensory receptors sense a body shift that the visual system cannot detect. The postural control system then tolerates larger sway movements to the extent that visual stimuli become suprathreshold. Thus, the increased sway reflects the physiological limits of visual postural control inputs. This also holds for fore–aft sway, in which the retinal images vary in size with the sway. Involvement of eye torsion––in which the retinal shift is independent of the distance between eyes and 42

object––can have consequences for postural control only in rotational sway amplitudes (Fig. 4).32 In fact, fore–aft and lateral body sway as measured by posturography increased with increasing eye–object distance.36 In the latter experiments, the relative increase of fore–aft body sway was more pronounced than that of lateral sway. This difference may be explained by partial visual stabilization based on retinal displacement of the environment in the roll plane. Postural balance was undisturbed if nearby stationary contrasts in the periphery of the visual field were provided while individuals fixated remote targets. The increase in body sway amplitudes at heights introduces a real danger of falling from high places. Teleologically, it is a meaningful warning signal to the body to withdraw from stimulus situations that cannot be adequately perceived in terms of the space constancy necessary for postural control.32 This broadly gene-linked depth avoidance, known as visual cliff behavior, has been comprehensively studied by Walk and Gibson41,42 in animal species as well as humans. Pathological imbalance of stance and locomotion due to visual height intolerance and acrophobia The assessment of threat and anxiety is an integral component not only of orientation but also of postural control and locomotion in health and disease.43 Several studies have investigated the impact of acrophobia on body posture44,45 as well as a height threat on healthy individuals standing in a high place.46,47 Normal subjects exhibit a cautious way of walking when being visually exposed to heights as well as when only being aware of them in the absence of visual exposure.48 This led the authors to conclude that the mechanisms disturbing locomotion and balance occur at a high task level, at which cognition based on prior experience is integrated with sensory inputs. The aim of our own study was to explore the alterations in postural control and muscle activity that occur in individuals susceptible to visual height intolerance during height exposure and to determine the kind of visual stimulation and/or anxiety causing these alterations.49 We therefore evaluated balance control in susceptible individuals while standing on an emergency balcony 15 m

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Object

Fore–aft Sway

Mediolateral Sway

~ Roll Sway Figure 4. Visual control of body sway in fore–aft, mediolateral, and roll planes. Differential effects of head and body sway on the shift of the retinal image of a viewed stationary object. Angular displacements on the retina caused by fore–aft and lateral head displacements are smaller, the greater the distance is to the object. When exposed to heights and large distances, the head sway goes visually undetected, i.e., visual stabilization of posture is impaired in the fore–aft and lateral planes. This is different for head and body sway in the roll plane (bottom). In this plane, the distance between the eyes and fixated objects has no influence on the net retinal slip on the retina (i.e., visual stabilization of roll sway is not impaired). Modified after Ref. 32.

above ground level versus standing on ground level in the posturographic laboratory. Stimulusand attention-dependent changes in postural control were evaluated by a comprehensive stance protocol, including different visual feedback conditions (eyes open versus eyes closed; head upright versus head extended or flexed; see Fig. 1) and cognitive dual tasks. To disclose the different neuromuscular mechanisms underlying postural

control, we combined posturography with simultaneous electromyographic recordings of antigravity muscle innervation (Fig. 1, bottom right). A stabilogram diffusion analysis was also performed. It models the center-of-pressure trajectories during quiet stance as a process of coupled, correlated random walks and analyzes the diffusion properties of the process. This analysis shows that spontaneous body sway is typically characterized by a

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two-part behavior: open-loop control governs body sway over short-term intervals, whereas closed-loop control regulates it over long-term intervals.50,51 The open-loop system operates without sensory feedback and determines the steady-state activity of the antigravity muscles.52 Open-loop feedforward control thus represents the motor commands that place the body in a desired posture. In contrast, closedloop control relies on sensory feedback to correct drifts away from the desired posture.49,50,53 During height exposure—as compared to standing in the laboratory––susceptibles to visual height intolerance exhibited a stiffening of the musculoskeletal system. This was indicated by an increased open-loop diffusion activity of body sway and a lowered sensory feedback threshold for closedloop postural control.49 The altered postural control mode was associated with increased co-contraction of the antigravity leg and neck muscles. Similar changes in leg muscle activity were reported earlier in healthy individuals when standing exposed to height threat.46,47 In our study, body sway and muscle co-contraction correlated with the severity of perceived anxiety. These alterations of postural balance and muscle activity were diminished if nearby stationary contrasts were visible (head flexion) or if individuals closed their eyes. The performance of a cognitive dual task also improved impaired balance.49 In another study on susceptible individuals, video-analysis of locomotion on an emergency balcony showed that their mean locomotion speed was slower than that of unsusceptible individuals.27 The slower speed was related to smaller step frequencies and step lengths, which correlated moderately with subjective fear. These data confirm earlier human laboratory experiments with healthy individuals who walked on a narrow walkway at a height of 3.5 m compared to ground level.48 The locomotion of susceptible individuals when exposed to heights is clinically best described as slow and cautious, broad based, and consisting of small steps. Moreover, susceptible individuals appear to walk with flat-footed contact and show less dynamic vertical oscillation of body and head.27

behavioral effects on (1) eye movements, (2) head movements, (3) posture, and (4) locomotion. These motor reactions of reduced eye and head movements, a body sway with smaller amplitude, but higher frequency, and a cautious, slow locomotion do not result from less muscle activity. On the contrary, they are caused by the co-contraction of antagonistic, especially antigravity, muscles in the neck and legs, possibly also of the extraocular eye muscles. Common colloquial expressions best depict this “motor pattern of fear at heights”: those who experience an extreme threatening stimulus or anxiety are said “to be scared stiff” or “to freeze.” This pattern might resemble the primitive reflex of feigning death that can be observed throughout nearly the entire animal world including humans. In biology, it is mostly defined as defensive behavior. When escape is impossible, a prey animal feigns death in the desperate hope that the predator attacks only living prey. It is commonly referred to as tonic immobility. One of the first descriptions of this phenomenon was published in Science in 1893.54 The author reported that a snake when threatened had turned onto its back and stiffened, remaining so until the danger passed. Other species have also shown stiff immobilization when feigning death.55 While serving to support the birth process in babies, the fear paralysis reflex is one of the so-called primitive reflexes still present in humans. Some have even proposed the refutable hypothesis that it might cause the sudden infant death syndrome after birth.57 The following is a typical description of feelings of immobility by patients with acrophobia: “ . . . when it gets really bad, then I can’t even lift my foot. It’s like my feet are glued to the ground. I’d probably remain standing there forever, for I can’t move my legs.”56 To draw a comparison between stiffening of postural control at height and tonic immobility in the face of an attacker might be rather a stretch. We would certainly not go so far as to say that the motor behavior observed in our experiments can be compared with an atavistic variant of feigning death. However, certain aspects such as co-contraction, freezing, and slowing of locomotion resemble this primitive motor behavior.

Scared stiff by acrophobia: an atavistic motor reaction resembling feigning death?

Acrophobia and phobic postural vertigo: two disorders with fall-free fear of falling

The exposure to heights of individuals susceptible to visual height intolerance or acrophobia has typical

Anxiety appears to be the critical symptom causing the ocular motor, balance, and locomotor

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Acrophobia impairs exploration, stance, and gait

Figure 5. Acrophobia and phobic postural vertigo are two disorders that share anxiety of falling as a major symptom although those afflicted do not fall. Both are characterized by an individual susceptibility to the condition. In acrophobia, individuals often have had earlier experiences at heights, whereas in phobic postural vertigo the experiences are often initiated by a vestibular disorder. The provoking stimuli are disease specific, but both end in a common circular cascade of symptoms, the so-called vicious circle or circulus vitiosus (bottom). Anxious concentration on control of postural stability triggers co-contraction of the antigravity muscles, thereby causing an inadequate mode of interaction between open- and closed-loop mechanisms within the postural control systems. This leads to subjective imbalance, which in turn enhances anxious control of posture. Modified after Ref. 60.

reactions in susceptible individuals when exposed to heights. The question arises as to whether the motor behavior is typical and specific for acrophobia or simply reflects an unspecific reaction to anxiety in general. We have also studied postural sway and locomotion in another condition, in which fear of falling is one of the central complaints: phobic postural vertigo.58 This syndrome is characterized by a combination of postural dizziness/vertigo with subjective instability of stance and gait in patients who achieve normal neurological results on balance tests. Both conditions, acrophobia and phobic postural vertigo, are characterized by fear of falling. They simply differ in severity. The first is a life-threatening anxiety of plunging into the depths, the second a fear

of falling down (Fig. 5). However, they both share two other criteria: there is dissociation between the subjective and objective risk of falling, and typically both conditions do not lead to an increased number of falls compared to normal controls. Patients with phobic postural vertigo were tested with the same methods in order to measure their balance performance during upright stance and locomotion. The results were almost identical to those of individuals susceptible to acrophobia. Their postural control was characterized by a less complex, that is, more constrained and regular, mode of standing59 accompanied by an inadequate interaction between openand closed-loop control mechanisms, indicating a stiffening of the musculoskeletal system and a

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lowering of the primary sensory feedback threshold.60 This finding confirmed earlier observations on body sway during tandem stance61 and during visually induced roll vection in patients with phobic postural vertigo.62 Co-contraction of the antigravity muscles and inadequate interaction between openand closed-loop postural control culminate in a circular cascade of symptoms or a so-called vicious circle (circulus vitiosus) of postural instability common to both conditions (see Fig. 5). Thus, the stiffened posture in both conditions suggests a final common pathway of sensorimotor control of balance. Also, the gait pattern of susceptible individuals to fear of heights when exposed to height does not appear to be specific, because similar alterations have been described as a slow, cautious gait in patients with phobic postural vertigo.63 It even corresponds to the wary gait observed in children and adults with visual deprivation.64,65 Finally, psychiatric data indicate that acrophobia and phobic postural vertigo also share the higher comorbidity rates of anxious and depressive disorders.2,66

Tips and recommendations for coping strategies and prevention of visual height intolerance and acrophobia Acrophobia arises when physiological height imbalance or height intolerance induces a conditioned phobic reaction characterized by a dissociation of the subjective and objective danger of falling. Although the acrophobic patient also recognizes this discrepancy, he/she can typically only with difficulty overcome the “panic anxiety,” which is accompanied by vegetative symptoms and inappropriate avoidance behavior. The above-discussed experiments of visual exploration and balance control of stance and locomotion in susceptibles allow us to recommend the following guidelines for coping strategies to avoid or minimize acrophobia under natural stimulus height conditions (Table 1).32,67 These recommendations may also be used as an add-on to current behavioral therapy strategies; however, they must still be investigated in treatment trials. Prospective treatment studies are also necessary to test their efficacy in the long run because psychotherapists are well aware that such actions might reinforce rather than extinguish acrophobic behavior. 46

Table 1. Recommendations for behavioral coping strate-

gies of visual height intolerance. Vision

Fixate the horizon Look at near stationary contrasts When looking into an abyss, keep near stationary objects in sight in the peripheral field of vision in order to maintain visual control of posture Avoid large-field motion stimuli (for example, clouds) that can lead to visually induced illusory motion Do not look through binoculars without some kind of support/stabilization (misleading visual motion stimulus) When standing, you may close your eyes for a while (to reduce anxiety)

Position

Sit down or lie down (symptoms maximal when standing, minimal when lying) Lean on something, hold tight to something

Locomotion Pause or stop walking (symptoms increase with locomotion at heights) Cognition

A cognitive dual task (e.g., naming items from a given category) reduces anxiety and improves balance during stance and locomotion

Acknowledgements The authors thank Judy Benson for copyediting the manuscript. The work was supported by the Federal Ministry for Education and Science of Germany (BMBF 01 E0 0901) and the Hertie Foundation. Conflict of interest Two authors, T.B. and G.K., are shareholders of the EyeSeeTec GmbH, which builds the binocular infrared camera used for measuring eye movements. References 1. Huppert, D., E. Grill & T. Brandt. 2013. Down on heights? One in three has visual height intolerance. J. Neurol. 260: 597–604. 2. Kapfhammer, H.P., D. Huppert, E. Grill, et al. 2014. Visual height intolerance and acrophobia: clinical characteristics and comorbidity patterns. Eur. Arch. Psychiatry Clin. Neurosci. doi: 10.1007/s00406-014-0548-y. 3. Depla, M.F., M.L. ten Have, A.J. van Balkom, et al. 2008. Specific fears and phobias in the general population: results

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Acrophobia impairs visual exploration and balance during standing and walking.

This review shows that persons with visual height intolerance or acrophobia exhibit typical restrictions of visual exploration and imbalance during st...
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