Keywords
anticipation; random events; pupil dilation; emotion;
anticipation; random events; pupil dilation; emotion;
The main revisions to Version 1 are:
A comment to each of the reviewers is posted in the comments section of the online version.
The main revisions to Version 1 are:
A comment to each of the reviewers is posted in the comments section of the online version.
See the authors' detailed response to the review by Leo McHugh
See the authors' detailed response to the review by Chris Baker
The anticipation, or prediction, of future events is a fundamental activity of our conscious and implicit, (i.e. unconscious) cognitive abilities. To be able to predict, even approximately, future movements, perceptions and events, reduces the risks and harms of a future threatening situation and more importantly, optimizes the use of our limited cognitive and energetic resources (e.g. Friston1).
It is therefore not surprising that the study of anticipation has become an interdisciplinary line of research encompassing psychophysiology and neurophysiology (e.g. Van Boxtel and Böcker2), cognitive processes (Barcelo, Bestmann and Yu3) and artificial intelligence (Butz, Sigaud and Baldassarre4).
At the core of the anticipatory activity is an innate sensitivity to the structure and statistics of the environment in order to build up correct representations of each event in order to prepare the organism to perceive and act in a way that minimizes errors and reduces unnecessary adjustments (e.g. Clark5). But this raises the question of how it is possible for the organism to prepare for future events if they are unpredictable or equally probable?
Our interest is focused on this more extreme form of anticipation, that of random events. Even if the study of predicting unpredictable events seems a paradox, there is cumulative evidence related to almost 15 years of investigation, that humans, and perhaps every other living organism, can predict some classes of events above the level expected by chance (see the meta-analysis by Mossbridge, Tressoldi, and Utts6). If proven, this phenomenon will further enhance our knowledge about innate predictive survival abilities.
In this study, we demonstrate that pupil dilation (PD) reactions differ before the random presentation of a neutral or a potentially threatening stimulus.
Similar to other psychophysiological variables (e.g. heart rate, skin conductance, etc.), PD reacts to different emotional states that are correlated with the arousal of the autonomic sensory system (e.g. Bradley et al.7). Because the pupil dilates with sympathetic activity and constricts with parasympathetic activity (Beatty and Lucero-Wagoner8; Steinhauer et al.9), it represents an accurate and unobtrusive measure of the cognitive resources invested in a task, for example in doing arithmetic tasks.
An interesting application of PD is shown in tasks where participants are not consciously aware of some information but their PD reveals that it is unconsciously available and is being processed by the cognitive system. For example Bijleveld, Custers and Aarts10, used PD to reveal the strategic recruitment of resources upon presentation of subliminal reward cues.
However PD not only gives information about unconscious cognitive activity but can even anticipate future perceptual or cognitive activities. Einhäuser, Stout, Koch, and Carter11 used PD to reveal perceptual selection and its prediction of subsequent stability in perceptual rivalry and Einhäuser, Koch, and Carter12 employed PD to reveal decision making before a person voluntarily reported it.
Starting from these studies and the cumulative evidence that the human psychophysiological and electrophysiological systems react differently before random presentation of two categories of emotional stimuli such as pictures, sounds, etc. (Mossbridge, Tressoldi, and Utts6), we aimed to further investigate whether PD can actually predict random events at the level of each single trial of each participant (see Procedure). An increase of approximately 20% of alerting sounds above the mean chance expected (MCE) has already been observed by Tressoldi et al.13 in the prediction of auditory alerting and neutral sounds presented randomly at the level of single trials (a summary of results obtained in that study is presented in Table S1 in the Supplementary Material of this paper).
In this paper, we will present the results of a conceptual replication using visual information contrasting a potentially “threatening” stimulus with a neutral one using an experimental procedure that simulate an ecological condition where a dangerous or a neutral event could happen randomly.
Participants were recruited by advertisements mainly among students of Padova University. Exclusion criteria included uncorrected vision and use of drugs that could affect pupil size and pupil dilation. These characteristics were ascertained by asking each participant.
Estimating an effect size of approximately 0.30, to achieve a statistical power above 0.80, setting α=0.05, an opportunity sample of 100 students and personnel from Padova University (Faul et al.14) were recruited by a research assistant to participate in an experiment on a gambling task. The final sample comprised 32 males and 68 females with a mean age of 29.3 and with a standard deviation of 3.8.
Participation inclusion followed the ethics guidelines in accordance with the Helsinki Declaration and the study was approved by the Ethics Committee of Dipartimento di Psicologia Generale, the hosting institution. Before taking part in the experiment, each participant provided written consent after reading a brief description of the experiment.
The experiment consisted of two different phases, a preliminary and a formal one. The preliminary phase aimed at familiarizing each participant with the procedure and testing if they reacted differently to the two stimuli.
Each participant was seated in front of a 19 inch monitor in a sound and light attenuated lab of approximately 120 cd/m2 measured with a Minolta light meter.
Before the formal sessions, each participant was told: “Before the formal experiment, we must record your personal pupil dilation reactivity to the two types of stimuli you will see behind the door. You must simply watch what will happen on the screen without doing anything. When the door opens, you will see a gun shooting at you, hearing a shot, or you will see a smile. You will see the shooting gun and the smile ten times each, in random order”.
We chose to limit the test to 10 trials per stimulus to avoid boredom and reduce the possibility of using controlled strategies to predict the target.
If there was no need for further clarification, the task started with the calibration of the eye position for the Eye Tracker apparatus. This consisted of participants following a dot moving slowly in different positions on the monitor in a natural way without the need to fix the head position.
Once the calibration was completed, the task started with the stimuli presentation. The sequence of events is presented in Figure 1. The inter-item interval was randomly chosen between 2 and 4 sec.
The two target stimuli, the gun and the smile, and the door, were calibrated for luminance (300 × 471 pixel; 72 horizontal and vertical dpi). The door was colored in black similar to the video background to avoid PD modification consequent to differences in luminosity. Their luminance measured using cd/m2 with a Minolta® photometer was, for the gun: 15 center, 90 periphery, Smile: 73 center, 4 periphery, door: 48 center, 8 periphery.. taken at fifty centimeters from the monitor. After the preliminary phase, the formal phase started.
The research assistant’s instruction to each participant was: “Now your task is to let your pupil dilation predict what you will see behind a closed door that will be shown in the center of the monitor. Behind the door you can see a gun shooting at you or a smile. The computer will monitor your pupil dilation and will predict for you what you will see. Remember that the choice of the shooting gun and the smile, is completely random and hence it is not possible to find an underlying rule to predict their sequence. The task consists in two sessions of 10 trials each. For each correct hit you will earn 0.5 euros”.
The sequence of events is presented in Figure 2. In this case pupil dilation was measured for 5 seconds during the fixation of the door and used to calculate the prediction accuracy (see Individual prediction accuracy paragraph) .
Eye-Tracker Apparatus: The eye-tracker model Tobii T120®, Tobii, Stockholm, has the following technical characteristics: data rate, 120 Hz; accuracy, 0.5 degrees; freedom of head movements, 30 × 22 × 30 cm; monitor, 17 inch; 1280 × 1024 pixels; automatic optimization of bright-dark pupil tracking. PD is measured automatically in millimeters by the apparatus using the incorporated near infrared detectors and software. These data were fed to an original software for their storage. This program, created using E-Prime™ v.2.0, written by two of the authors (MM and LS) and interfaced with the eye tracker, controlled events presentation and pupil size automatic recording. The source code is available at: dx.doi.org/10.6084/m9.figshare.848604.
The sampling with replacement of the two stimuli in the two series of ten trials was randomized using E-Prime™ v2.0 randomized statement and Random function which was reset after every trial. This procedure guarantee against the possibility to guess the incoming stimulus by learning implicit and explicit rules.
The light in the laboratory was constantly dim, approximately 30 cd/m2 to avoid undesired or unrelated changes to the participants’ pupils.
The time necessary to complete the calibration, 2 min on average and give the instructions to participants was long enough to accommodate their pupils to the ambient light before starting the experiment.
We used both a frequentist parameters estimation and a Bayesian model comparison approach, according to the American Psychology Association (APA)15, Kruschke16 and Wagenmakers, Wetzels, Borsboom and van der Maas’s17 statistical recommendations.
This statistical approach is recommended to limit the shortcomings of the classical Null Hypothesis Significant Testing (e.g. Tressoldi et al.18). Basically, each parameter of interest (mean, correlation, etc.) is estimated for its precision by the confidence intervals, and its effect size or Bayes Factor. For those interested in the classical statistical significance with this approach, it sufficient to check if the confidence intervals include (not significant) or exclude (significant) zero.
Inferential frequentist estimates were applied both to the sum and the average of correct guesses (hits) using a binomial and a one-sample t-test statistical test respectively to take in account the sum and the percentages of hit responses. Confidence intervals were estimated using a bootstrap procedure based on 5000 samples.
We adopted a model comparison approach contrasting the alternative hypothesis of a higher difference with respect to MCE (H1) with the Null Hypothesis (H0) of a nil difference with respect to the MCE. We calculated the Bayes Factor (BFH1/H0) using the software implemented by Morey and Rouder19 for the comparison with the one-tailed one-sample t-test, applying Jeffreys, Zellner, Siow (JZS) prior (see Jeffreys20) setting an effect size of 0.3, as suggested by Rouder et al.21.
Before proceeding with the statistical analyses, the data for each participant were screened for artifacts. All artifacts, i.e. missing or anomalous (PD values close to/below 1, or above 10) data recordings related to PD easily detected by inspecting the raw scores saved in the individual files, were eliminated. If they exceeded the threshold of 60%, that is 12 out 20 trials, the entire participant was excluded and substituted to keep the total sample equal to 100. The overall percentage of artifacts was 4%. The full raw data and corrected for anomalous data are available at http://dx.doi.org/10.6084/m9.figshare.818978 (Tressoldi)22.
In order to take into account individual differences, we standardized the PD values related to the 20 trials measured in the anticipation phase to z scores for each participant. Next, the means associated with the two stimuli chosen by the software were calculated. In this way a mean was always above zero and the second one below zero except in the case of identical mean between the two stimuli. The prediction for each trial was obtained simply by defining whether the value of PD, above or below zero corresponded to the stimulus that was chosen randomly. For example, if the PD standardized means associated with the smile and the gun were respectively 0.25 and -0.15, each PD value above zero predicted a smile and vice versa, each value below zero predicted a gun. At the end of the trial, the sum and the percentage of hits (correct predictions) were calculated for each participant.
In Table 1 we report the descriptive statistics, in Figure 3 the hits percentages with their 95% Confidence Intervals (CIs). and in Table 2 the effect sizes estimation and the BFH1/H0 of the two stimuli and overall with respect the MCE with the corresponding 95% CIs.
(n=100).
Hits | Smile | Gun | Overall |
---|---|---|---|
Mean % | 0.549 | 0.569 | 0.559 |
SD | 0.28 | 0.16 | 0.94 |
SUM | 508/931 | 554/986 | 1062/1917 |
Effect sizes with 95% CIs and BFH1/H0 values of hits percentage for the two stimuli and overall with respect the MCE = 50%.
The means estimate related to both stimuli and overall, show clearly that the prediction accuracy is above the mean chance expected of 50%.
The estimates of all effect sizes, both those referred to the binomial test and to the one-sample t-test, are above zero and in the range of medium effects. Furthermore the BF values range from 6 for the smile to 284394 for the overall accuracy.
It is plausible to expect a correlation in the difference between the anticipatory PD associated with the two stimuli and their prediction accuracy. The variance explained by this correlation is R2=0.348, 95%CI: 0.20 to 0.49. This moderate correlation suggests that anticipatory PD differences between the two stimuli explain only a part of the hits or correct predictions. This finding will be commented on further after the results of the exact replication.
Expectation bias, arises when a random sequence including multiple repetitions of the same stimulus type (e.g., five non-arousing stimuli) produces an expectation in the participant that the next stimulus should be of another type (e.g., an arousing stimulus) and the contrary (the Gambler’s Fallacy). In the Figure S1 in the Supplementary Material we report the trend observed for the two types of targets. Ninety-eight percent of all series of identical stimuli were comprised between 1 and 5. The visual inspection supported by the estimate of the linear trend, -0.0071 for the smile and -0.0128 for the gun, excludes an expectation bias for both the stimuli.
The overall prediction accuracy turned out above 50%, the chance expected. Even if of small magnitude in absolute terms, approximately 5%, the parameter estimates suggest that this is quite substantial in term of effect size and BF.
Before commenting further on these findings we wanted to test their reliability in an exact replication of the experiment.
Following the suggestions of Wagenmakers et al.23 and of the Open Science Collaboration24, the experiment was registered on the site http://www.openscienceframework.org before data collection.
We preplanned to recruit the same number of participants as in the original study assuming a similar effect size and setting the statistical power to 0.80. The final sample recruited as in the first experiment, comprised 26 males and 74 females with a mean age of 23.02 with an associated standard deviation of 2.7.
In Table 3 we report the descriptive statistics, in Figure 4 the hits percentages with their 95% CIs and in Table 4 the effect sizes estimation and the BFH1/H0 of the two stimuli and overall with respect the MCE with the corresponding 95% Cis.
Hits | Smile | Gun | Overall |
---|---|---|---|
Mean % | 0.578 | 0.596 | 0.587 |
SD | 0.16 | 0.14 | 0.09 |
SUM | 533/943 | 536/911 | 1069/1854 |
Effect sizes with 95% CIs and BFH1/H0 values of hits percentage for the two stimuli with respect the mean chance expected, 50%.
The means estimates related to both stimuli and overall, show clearly that the prediction accuracy is above the mean chance expected of 50%.
The estimates of all effect sizes, both those referred to the binomial test and to the one-sample t-test, are above zero and in the range of medium to large effects. Furthermore the BF values range from 2317 for the smile to 1.5 × 1013 for the overall accuracy.
The correlations between the difference between the anticipatory PD associated with the overall prediction accuracy was R2=0.42, 95%CI: 0.27,0.56, overlapping that observed in the original experiment.
The same analysis used in the original experiment yielded similar results (see Figure S2 in the Supplementary Material), showing no sign of expectation bias.
In this replication, the hit percentages of the two stimuli and the overall hit percentage are slightly larger, as well as the effect sizes and BFs estimates, confirming the results of the original study. The BFs in this case are superior to those observed in the original study and in the range of extreme evidence according to Jeffreys20 criteria.
The difference between the anticipatory PD associated with the two stimuli predicts approximately one third of the variance related to the overall accuracy. At present we do not have hypotheses about which other predictors can contribute to the remaining variance.
The results of the two experiments support the idea that PD can predict future random stimuli therefore adding more evidence to the findings reported by Tressoldi et al.13 using auditory stimuli.
Even if these results were due to unpredicted methodological or statistical artifacts, as in all experiments, we can rule out that in our case they are a due to an improper randomization algorithm, the characteristics of our participants or a fault detection of PD by our apparatus.
The observed estimated prediction accuracy is between 5 to 10% above the chance level expected. It remains to be explored whether the 5 to 10% above chance represents an upper limit of this prediction or whether it can be enhanced.
It seems then that PD can be implicitly (unconsciously) modulated to predict random and hence statistically “unpredictable” events. Even if of small magnitude, this predictive ability could have important adaptive consequences, for example in cases of serious threats to life, suggesting that this characteristic is another expression of the powerful adaptive functions of our psychophysiological system that can anticipate future events, for example by promoting advantageous decision-making (e.g. Denburg et al.25), anticipating a reward (e.g. Hackley et al.26) and the pain of others (e.g. Caes et al.27).
It seems that PD, like possibly all other apparatuses regulated by the psychophysiological system (i.e. heart rate, skin conductance level), has innate characteristics specifically dedicated to the anticipation of future events, no matter how predictable, extending the potentialities of survival mechanisms.
The investigation of the mechanisms at the base of this capacity is an open question. If random events cannot be predicted using previous experiences and information, we can argue that some “guessing” mechanisms based on probabilistic estimations are adopted. For example, we are currently testing if our results can be modeled using the Bayesian hierarchical generative model suggested by Mathys, Daunizeau, Friston and Stephan28 to investigate individual learning under uncertainty.
Another hypothesis is the possibility that our psychophysiological system can manifest a sort of temporal quantum-like entanglement, restoring brief time-symmetry situations, apparently violating the past to future flow of time, allowing a connection between present and immediately future events like those observed in quantum physics (e.g. Ma et al.29) and recently studied in the perception of ambiguous images by Atmanspacher and Filk30.
The fact that it is possible to study this characteristic at the level of a single trial taking into account individual differences, opens up the possibility of devising proof of concept experiments for potential possible applications to be adopted in real life. For example, it is not very complicated to devise technical devices to add to glasses or a smartphone for instance, that can amplify the subtle variations of PD at the level of a conscious overt detection in a way to be used intentionally by every person or to use these variations to activate automatically an alarm that could enhance personal safety when driving or walking.
However only independent exact or conceptual replications can support our findings, for example changing the type of stimuli and/or the randomization algorithm.
Authorship: P. Tressoldi developed the study concept. M. Martinelli and L. Semenzato, devised the software. All authors contributed to the study design. Testing and data collection were performed by two research assistants. P. Tressoldi performed the data analysis and interpretation. All authors approved the final version of the paper for submission.
We acknowledge the relevant advices offered by Dick Bierman, Eva Lobach, Dean Radin and Julia Mossbridge in particular on how to analyse the anticipatory signals and Maaike Pols for revising the English.
Error bars represent the 95% confidence intervals.
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Competing Interests: No competing interests were disclosed.
Competing Interests: No competing interests were disclosed.
Competing Interests: No competing interests were disclosed.
Competing Interests: No competing interests were disclosed.
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