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Dec 11, 2017 - Keywords - heart rate variability, acute stress, ophidiophobia. I. INTRODUCTION. Some snakes are venomous, therefore the fear of snakes is.
Heartbeat Interval Dynamics in Response to Acute Stress in Human: A Case Study of Real Fear of Snake Viktor Avbelj* and Maja Brložnik** *Department of Communication Systems, Jožef Stefan Institute, Ljubljana, Slovenia ** Small Animal Clinic, Veterinary Faculty, University of Ljubljana, Slovenia [email protected], [email protected] Abstract - Heartbeat dynamics changes promptly and substantially in response to acute stress. This is due to direct neural connection of the heart and the central nervous system. An opportunity to analyze a video recording synchronized to a simultaneously recorded ECG arose after preparation of educational TV show about adrenaline. Although the scenario for the experiment in Ljubljana Zoo did not presume to expose a person to acute fear, the unexpected situation of awareness of proximity of the snake’s head led to actual sudden acute fear of the snake for the third time in person’s life. This case study presents heartbeat dynamics before and during acute fear phase. The response of the heart to acute fear was immediate. Large and fast variations of heartbeat intervals were observed throughout the whole experiment (heartrate decrease by up to 32 beats/min in 5 seconds), indicating upheaval in regulation of cardiovascular parameters. Keywords - heart rate variability, acute stress, ophidiophobia

I.

INTRODUCTION

Some snakes are venomous, therefore the fear of snakes is effective in a sense that a person reacts quickly to avoid danger. From the evolutionary point of view, it is clear that a quick response is more important than a precise identification of real danger. Even if a person is convinced that there is no real danger, the mechanism of reflex reactions takes priority in human response [1, 2]. It is believed that the fear of snakes occurs in about one third of adults [3]. The exaggerated fear of snakes is called ophidiophobia [1]. It is one of the most common specific phobias. Detection of snakes in visual search tasks has been shown to be more rapid than detection of other tested objects [4]. It has been shown that even 6-month old infants reacted with pupillary dilation when presented with pictures of snakes [3]. The non-arbitrariness of the snake fear, in combination with the evolutionary relevance of snakes to human survival, lead to the postulation that humans are evolutionarily “prepared” to fear certain stimuli over others [1, 2, 5]. However, many researchers failed to replicate some of the findings supporting the so-called Preparedness Theory and have criticized the contextual relevance. Furthermore, methodological and interpretative limitations have been addressed [1, 6]. Neither have various cultural differences been studied. Therefore present understanding implicates that fear of snakes is primarily learned through cultural transmission [1, 6].

The author Viktor Avbelj acknowledges the financial support from the Slovenian Research Agency under the grant P2-0095.

One of the reactions to acute fear is an accelerated heartbeat. In this case study, we analyze ECG and video recordings from TV cameras, soundtracks included. The recordings were made during preparation of TV show and the experiment was therefore not specifically prepared for the purposes of this case study; only after a thorough examination of the recordings two months later such a possibility was noticed. The acute fear was unmotivated; the response to acute fear was genuine and could not have been achieved in controlled experimental conditions. Such an experiment would have been even unethical. In this case study, we analyze the heart rate variability at the time when the person was preparing to take a nonvenomous snake in her hands, during the time when she held the snake in her arms and at time when the acute fear of snake was triggered due to an unexpected movement of the snake's head. Furthermore, the heart rate variability during the experiment is compared to person’s heart rate variability at rest. II.

MATERIALS AND METHODS

A. The person and the snake in the experiment The experiment in Ljubljana Zoo has been made for the educational television show about adrenaline ("Osvežilna fronta", RTV Slovenia, released on 11th December, 2017). The person involved in the experiment later described that she has had the fear of snakes ever since she remembers. This fear was likely learnt by way of listening to the fairytales and her grandmother's stories about snakes. She saw a snake for the first time in her life when picking up mushrooms in the woods at the age of eight. She got frightened as she nearly stepped on it. The snake was lying still on the ground, and then raised its head when unexpectedly approached. The second experience with a living snake happened 5 years ago, when she got scared again while preparing a contribution for TV Slovenia on overcoming the fear of snakes. The 3rd experience is described in this paper (Fig. 1). The snake called Greta is a female python (Python regius, known as Royal python) that inhabits the Ljubljana Zoo. It is not venomous, and is not endemic in Slovenia. In Slovenian natural habitat, there indeed are snakes but are smaller, and few of them are venomous. B. ECG, video and audio recordings The ECG recording was made with Savvy ECG (Saving, Ljubljana), a single-channel ECG with long-term recording capability that communicates via Low Power Bluetooth with

the mobile phone [7]. We used the MobECG application (version 1.7.5.1, Saving, Ljubljana) on the LG K8 4G smartphone (using Android 6.0). On the day of the experiment the person was self-recording her ECG from 8:27 AM to 6:45 PM. We used an unfiltered recording, which in addition to the ECG included high frequency signals of muscle murmur and other artifacts also. The electrodes were installed at the V1 and V2 positions of the standard 12-channel ECG so that the device measured the voltage difference between the V2 and V1 leads. Ag/AgCl electrodes (Skintact, T60) were used. The ECG recording was then analyzed with the VisECG program (version 1.2.13, Jožef Stefan Institute, Ljubljana).

manually) was switching the LED on and off. In the next step, the synchronization accuracy was improved by comparing the ECG recording to the video clip. The sudden movements of the person (a clap and a fast up and down hand movement) are clearly identified in the video footage and the reflection of these movements can be identified in the ECG recording also (artifacts). This is how we improved the synchronization between the ECG and the clip to 1-2 video frames that is 4080 ms. Synchronization was time consuming, which could be avoided if the experiment had been planned for such image processing. The synchronization step could have been optimized by using a test generator and the LED in the same manner as done for the display of the smartphone and the LED. C. Experiment

Fig. 1: The female presenter a fraction of a second before noticing that the snake 'Greta' (Python regius) just moved its head closer to her left hand (see No. 9 in Fig. 2). The smartphone in the hands of her colleague shows real-time ECG from the wireless ECG sensor attached to her chest. Picture reproduced with permissions of both subjects

Video and audio were recorded for 5 minutes simultaneously with two professional TV cameras. The resolution of the images was 1920x1080, 25 frames/s, stereo audio channels were sampled with 48 kHz, all coded in MPEG4 format (picture 8 Mb/s, sound 189 kb/s). Videos were viewed with a program that also displays individual video frames (Vegas Movie Studio Platinum 9.0, Sony Creative Software Inc.). In the analysis of recordings we used only single camera footage, while the footage of the second camera was used only to verify the quality of synchronization between the ECG and the video footage of the first camera. ECG and video synchronization was accomplished in two steps. Rough synchronization was achieved by comparing the ECG recording with parts of the video, where the camera showed the screen of the phone with a display of telemetric ECG. In this step, we achieved synchronization with an accuracy of about 100 ms, because the ECG display on the phone lags 133-233 ms, which was measured with a test video (30 frames/s). The test clip simultaneously screened the phone with the signal from the ECG sensor and the LED (Light Emitting Diode), which was connected to the ECG sensor and to the pulse generator. This generator (we triggered it

As mentioned earlier, during the experiment the test subject (the female reporter pictured on Fig. 1) wore the one-channel ECG sensor, which was wirelessly sending a signal to the phone. At the beginning the test subject was getting accustomed to the presence of the snake. This phase lasted for almost 4 minutes (Fig. 2, No. 1 - 7); from the time the snake was taken out of the terrarium until the moment when the test subject claimed that she was no longer afraid. Shortly afterwards (15 s), the test subject took the snake into her own hands and again quickly handed it back to the demonstrator due to the unexpected movement of the snake. In her own words, the test subject corroborated that she did not remember precisely whether she either saw the movement of the snake's head or felt the move. The video footage demonstrates that the person was not looking directly at the snake but rather at the phone displaying her ECG. Only her left eye was in such a position that her peripheral vision may detect the movement of the snake's head. To study the effect of adrenaline the TV show also features measurements of the force by which a person can compress a dynamometer, but these measurements are not presented in this case study.

Fig. 2: Heart rate during a 5-minute video recording. Large variations of heart rate in intervals of less than 10 seconds are visible. 1) The snake is taken from the terrarium. 2) The test subject touches the snake for the first time. 3) The test subject touches the snake for the second time. 4) The test subject contracts the dynamometer. 5) The interval during which the test subject is getting used to sensation of touching the snake. 6) The test subject agrees to take the snake into her hands. 7) The test subject proclaims, "I'm not afraid." 8) The interval where the test subject holds the snake in her hands. 9) Acute stress event, when the snake suddenly moves its head, which scares the test subject

III.

RESULTS

All of the experimental phases correlated with the heart rate are presented in Fig. 2. From the time they take the snake from the terrarium (1), until the test subject first touches it (2), the

pulse is on average constantly growing. Simultaneously there is a high variability of the heart rate with a maximum range of 95 to 130 beats/min; the ascent occurred in mere 8 seconds. From that moment and up to the start of the interval 5 in Fig. 2, the average heart rate is decreasing. During this time the Zoo staff member is reassuring everyone by chatting about snakes not being slimy and that when showing a snake to a fearful person the snake’s head should be hidden. In the interval 5, the test subject constantly keeps her hand on the snake, thus reducing her fear to the point when accepting to hold the snake by herself (6). Fifty seconds later she even said that she was not afraid (7). Just before the beginning of the interval 5 the largest pulse rate drop occurred (from 111 beat/min to 79 beats/min in 5 seconds). From the beginning of the interval 5 to the beginning of the interval 8, the average pulse rate is about 98 beats/min, and high heart rate variability is still present, reaching another large deviation after point 6, when the pulse drops from 112 beats/min to 83 beats/min in 5 seconds only. Such fast changes can be a result of rapid activation of both branches of the autonomic nervous system (sympathetic and parasympathetic) that innervate the sinus node of the heart. In the interval (8) till the moment of acute stress activation (9), the amplitude of the heart rate variability was about 3 times smaller than before. Acute stress occurred when a person detected an unexpected movement of the snake (Fig. 3). The interval S in the image (the snake moved its head) is located with an accuracy of 40-80 ms with respect to the interval T. The test subject's reaction of shiver has a sharply defined start and end. Myopotentials presented here could be distorted, since the sampling frequency was 125 Hz, the low-pass filter before the A/D converter was 150 Hz (-3 dB), which means that the signal was under sampled. The first heartbeat (QRS complex in ECG) after acute stress event emerges during the interval T when the person felt the shiver. We here quote the test subject’s description of the stress event in the Slovenian language: "Zgrozila sem se, kar pomeni, da me je streslo, kot da bi me zazeblo, tako kot se prestrašiš. Vse je bilo zelo avtomatično, nič premišljenega, kače pa sem se želela rešiti čim prej. Skratka, v mojem spominu je, da sem videla/čutila premik in to me je prestrašilo tako, da sem se stresla in se želela čim prej rešiti kače". Translation: "I was horrified, meaning I shivered; it felt like getting cold, like when you are scared. Everything was very automatic, nothing rational; I just wanted to get rid of the snake immediately. Basically, as far as I can remember, I saw or felt the snake's movement, which scared me to such an extent that I shuddered and just wanted the snake gone". After the acute stress event, the heart rate increased, slowly at first and then after the 3th heartbeat, the biggest rise in the heart rate occurs (Fig. 4). At the time of the beat 4, the test subject has already relinquished the snake, and the frequency increased up to 138 beats/min in the 15th beat after the stress event. The effect on the sinus node was therefore the strongest in the time between the third and fourth beat that is from 1.2 to 1.7 seconds after the occurrence of the acute stress cause. It was taken into account that the influence of the autonomic nervous system on the sinus node is possible only before the P wave in ECG.

Fig. 3: ECG at the time of acute fear. In the interval S, which lasts about 0.2 seconds, the snake moved its head. This provoked an acute response, which first appears as the test subject's shiver, and is recorded by the ECG as myopotentials in the T interval (480 ms). The center of the S interval is taken as the reference time of the acute stress event

After the 5th beat the acceleration of the heart rate was reduced till the 9th beat, which was the first one after the stress with deceleration, indicating that parasympathetic influence was greater than the sympathetic one. Further to the 9th beat a fine interplay between the two branches of the autonomous nervous system can be seen in Fig. 4.

Fig. 4: Heart rate 10 seconds before and after acute stress event (time 0). The first consecutive 5 heartbeats and the heartbeats 9 and 15 after the acute stress event are numbered. The numbers 1–4 correspond to those shown in Fig. 3

In comparison the heart rate variability in the evening of the same day is presented in Fig. 5. The amplitude of heart rate variability in 20 s segments is smaller than during the experiment with the snake (Fig. 2).

Fig. 5: Heart rate during 5 minutes in the evening (around 6:15 PM)

IV.

DISCUSSION

In case of a stressful event like in this case, a part of the brain, the amygdala, sends a distress signal to the hypothalamus, which functions as a command center, communicating with the rest of the body through the nervous system. As expected in threatening situations, speed is significant. Therefore fear-related information reach the amygdala prior to any information from the visual cortex, and a fear response is initiated prior to conscious recognition of the threat [1, 8, 9, 10]. The fast amygdala response explains immediate and rapid increase in heart rate after acute stress event in our case study. Response to sudden threatening stimuli is mainly unconscious and is called startle reflex. It assists to protect vulnerable parts of the body and facilitates escape from sudden threat [11]. Startle reflex is systematically modulated by the organism’s ongoing emotional state. Subjects with specific fears show a greater startle potentiation [12]. Anxiety, a negative emotional response to threatening circumstances, is associated with elevated high blood pressure, increased heart rate and an enhanced respiratory rate [13]. Heart rate responses to trauma-related pictures contributed to the identification of individuals with posttraumatic stress disorder [14]. Startle responses are not modulated by ongoing emotional processes alone. The amplitude of the startle response is reduced when a non-startle stimulus is immediately preceding the startle eliciting stimulus [12]. All these and many other mechanisms influence physiological response of an individual. Defensive behaviors in animals and humans vary dynamically with increasing proximity of a threat, and in dependence upon the behavioral repertoire at hand. When the approaching threat was inevitable, attentive freezing was observed as indicated by fear bradycardia and potentiation of startle reflex. In preparation for active avoidance, a switch in defensive behavior was observed, characterized by startle inhibition, heart rate acceleration and a general sympathetic dominance to facilitate fight or flight responses. If the organism was again placed in a context where a threatening event has been experienced, precautionary behavior has been engaged. Response output was characterized by attentive freezing, accompanied by fear bradycardia and potentiation of the startle reflex [15]. It is worth mentioning that in our case person’s heart rate was already increased before the acute stress event due to snake’s presence. Beside the direct neural connection of the brain and heart there is also a hormonal regulation of the cardiac response to stressful event, which is slower but was in this case already present. After a distress signal is sent from amygdala and/or other parts of the brain, hypothalamus activates sympathetic nervous system and activates adrenal glands that release adrenaline into bloodstream. Circulating adrenaline has a number of physiological effects (faster heart rate, increased cardiac contractility, increased blood pressure, faster breathing, bronchodilation, increased blood glucose, and many more). Additional oxygen increases alertness and sharpens the senses, while increased blood glucose supplies energy to all parts of the body. Since our case study subject would like to overcome the fear of snakes it is reasonable to

assume that simultaneous parasympathetically mediated mechanisms persisted and influenced the heart rate. Fear response is initially beyond the conscious control, but conscious control can be quickly involved [16]. To our knowledge there are no studies to understand this interplay between cognitive and automatic responses in the acute fear phase. However, individual differences have been observed in the psychological and physiological reactions to traumarelated stimuli and it has been suggested that this depends on trauma encoding indicating the codependence between cognition and automaticity [17]. Fear bradycardia and freezing response are commonly reported in animals in the face of overwhelming threats [18, 19]. For fear bradycardia in humans an alternative explanation, increased orienting, is also proposed [17]. Heart rate variability, a physiological phenomenon of variation in time intervals between consecutive beats, may be a marker of cardiovascular health or an indicator of autonomic nervous system activity. Heart rate variability of healthy cardiovascular system is associated with its own chaotic nature due to a beat-to-beat regulation by opposite sympathetic and parasympathetic modulatory influences [13]. Furthermore, hormones also influence the heart rate variability. It is accepted that in case of increased heart rate, the heart rate variability decreases [13, 19]. This has, however, not occurred in our case; the amplitude of heart rate variability was higher the whole time of the experiment when compared to the heart rate variability in the evening when the heart rate was lower. As expected, the highest rise in heart rate emerged immediately after the acute stress event. Heart rate increased from 110 to 138 beats/min (difference of 28 beats/min). In comparison, in studies where only fear relevant pictures were presented to fearful subjects, a statistically significant difference of only 4 beats/min has been reported [12]. In our case fear bradycardia was not apparent. However, it might have been hidden in the slow increase of the first 3 heartbeats after the acute stress event. Only after the 3th heartbeat large rise in heart rate occurs. It is important to notice that in order to remain within the ethical standards, the acute fear phase achieved in this experiment was not planned and therefore could not have been accomplished in a controlled experiment. Acute stress induces the release of stress hormones, which have various detrimental effects on the organism like suppressing immune system [20]. Furthermore, chronic stress has been linked to pathogenesis of numerous diseases and disorders like insomnia, depression, anxiety, rheumatoid arthritis, cardiomyopathy, gastric ulcers, ulcerative colitis, infections, diabetes, cancer, and other. However, our findings may be studied further within the existing workshops designed to overcome stressful situations.

V.

CONCLUSIONS

We have demonstrated that a small wireless ECG device combined with video recording could be efficiently used in behavioral experiments. To the best of our knowledge, this is

the first example where the heart rate variability was measured during a real life response to the fear of snakes. The heart rate variability was shown to have been higher during the periods of high heart rate (stress) than during the period of low heart rate (relaxation), which was contrary to expectations and may be due to fast activation and deactivation (modulation) of the sympathetic and parasympathetic branches of the autonomic nervous system that innervate the sinus node of the heart. This predicament may fall into category of individual differences. Further studies are needed to explain either variations of individual differences or to adjust the explanatory model.

ACKNOWLEDGMENT The authors of this study acknowledge the assistance of Neža Prah Seničar, who described her experience in detail and also provided the TV footage. Also, we thankfully acknowledge RTV Slovenia for giving the permission to use their recordings. Last but not least we are thankful to Eva and Luka to help us with translation of a part of the manuscript.

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