The impact of luminance on tonic and phasic pupillary responses to sustained cognitive load
Introduction
Pupillary reactions independent of luminance have been linked to cognition since the early sixties (e.g. Hess and Polt, 1964, Kahneman and Beatty, 1966). The pupillary reaction can be divided into two components: tonic pupil diameter and phasic pupil response (Beatty, 1982b). Tonic pupil diameter reflects a sustained component of the pupillary response and is expressed as an absolute pupil diameter. Often, tonic pupil diameter is also used as basal pupillary diameter. In turn, phasic pupil response refers to a transient component of the pupillary response and is expressed as dilation relative to some basal pupil diameter. While the typical order of magnitude of the tonic pupil diameter is 1 mm, that of phasic pupil response is 0.1 mm. Many authors stated that the magnitude of phasic pupil response to a given task was independent of tonic pupil diameter (Beatty, 1982a, Bradshaw, 1969, Kahneman and Beatty, 1967). Thus, given the presumption of the independence of these two pupillary components, Beatty (1982a) concluded that it is possible to compare the phasic pupil responses issued from various set-ups and reported by different laboratories. Notably, in the review, he presented a table of quantitative comparison of qualitatively different cognitive tasks (memory, language, reasoning and perception). The table confronted the results obtained by different researchers and permitted to see that, for example, the storage in memory of four words makes the pupil dilate more than that of a multiplicand, which is roughly equivalent to retaining in memory two digits. According to the corresponding pupillary reactions, it also put an easy multiplication problem higher (phasic pupil response about 0.1 mm larger) than a hard auditory discrimination task. However, one may call in question such ordering assuming that multiplication of two digits is sometimes easier than detection of a deviant sound. Such task classification, using the magnitude of phasic pupil response as a marker of difficulty, would prevail but on one condition; if tonic pupil diameter does not impact phasic pupil response. Suppose, indeed, that tonic pupil diameter varies as a function of the experimental setup at one hand, and phasic pupil response depends on tonic pupil diameter at another. In this case, in order to compare results issued from different experimental setups one should first make sure that the conditions were the same or at least similar. The investigation of these questions is of an importance when using pupil reaction as a marker of stress or workload in ecological conditions where such factors as light are difficult to control. Because if there exists a strong relationship between tonic pupil diameter and phasic pupil response, the transportability of laboratory results into real life conditions for applications such as human factors in aviation needs a whole reflection apart.
The dependence of the extent of a physiological reaction to an event on the pre-stimulation basal level was named “law of initial value” in the fifties (Lacey, 1956, Wilder, 1967). Lacey (1956) postulated that a high autonomic excitation before a stimulus would affect the reactivity and diminish the response but did not refer to the pupil, talking rather about skin resistance, heart rate, blood pressure, muscle potentials, etc. Recently, a few mentions of this law appeared in pupillometric studies (Gilzenrat et al., 2010, Höfle et al., 2008, Van Gerven et al., 2004). Formulated in terms of tonic and phasic components of pupillary response, the law of initial value would postulate that a large tonic pupil diameter would imply a smaller phasic pupil response. On the other hand, Sokolov in his work on orienting response (1963) also distinguished tonic and phasic components. In particular, his model (including pupil dilation response) incorporated a response amplifier associated with general arousal (tonic state) which amplifies the phasic response. Thus, according to Sokolovian work, large tonic pupil diameter would imply a larger phasic pupil response. Afterwords, Jin (1992) reviewed experimental data and proposed that the law of initial value should be revisited as follows: “The higher the initial value, the greater the organism's following reactivity, although a tendency to reversed responses may occur when the initial value reaches its upper extremity.” Therefore, Jin proposed to consider the law of initial value as a restriction of pupillary dynamic range, i.e. when the pupil is already large, it cannot dilate further. Thus, the direction of the law is still questionable.
The tonic pupil diameter has numerous sources of variation (Tryon, 1975). For instance, it is modulated by general organism's arousal, sustained cognitive load, or light conditions, both ambient illumination and focal luminance. When tonic pupil diameter is modulated by vigilance state, an inverse relationship between tonic and phasic pupil diameters was found by Gilzenrat et al. (2010) in an auditory oddball task. The authors discussed this finding with regard to the law of initial value but considered it as exclusively mechanical. Therefore, the authors verified if the inverse relationship between tonic pupil diameter and phasic pupil response held true when tonic pupil diameter was modulated by light conditions and proved it false in that case. This finding was afterward confirmed by Murphy et al. (2011) also in an auditory oddball task and, more recently, by de Gee et al. (2014) in a perceptual decision-making paradigm and Knapen et al. (2016) in an auditory vigilance task. Steiner and Barry (2011), on the other hand, in their study on orienting reflex, found that vigilance state modulated tonic pupil diameter but not phasic pupil response. As for cognitive tasks implying working memory, Steinhauer et al. (2004) found that the phasic pupil diameter was modulated by ambient illuminance when engaged in sustained processing. More recently, Peysakhovich et al. (2015) found that the phasic pupil diameter was modulated by the screen luminance in a short-term memory task. Most recently, Pfleging et al. (2016) also studied pupillary response, manipulating illuminance and luminance during a cognitive task. However, the authors used a one-factor-at-a-time method that does not enable the investigation of the illuminance-luminance interaction and reported exclusively the absolute pupil diameter values making impossible to compare tonic and phasic pupil responses. Altogether, to be able to compare pupil reactions issued from different studies that maintain different light conditions, and to transport the laboratory results into real-life applications, it is important to investigate further the relationship between the tonic and phasic components of the pupillary response and the factors that modulate these components. The pupillometry literature still has not given a clear answer to these questions, and a further investigation is needed. To the best of our knowledge, no studies investigated the impact of luminance on the tonic and phasic components of the pupillary response during sustained cognitive load.
Therefore, in the present study, we manipulated the sustained cognitive load and the screen luminance. To explore both tonic and phasic pupil response and so that both components would reflect cognitive processing, we used the Toulouse N-back Task – a novel working-memory task that couples n-back task with mathematical problems solving. This paradigm has the particularity to combine sustained memory load during a block and transient stimulus processing during each trial. We did not manipulate the transient load, and the stimulus processing was equal for all conditions. The objective of the study was to investigate the impact of luminance on the tonic and phasic pupil response during various levels of sustained cognitive load. We assessed the following questions: a) How does the luminance impact both tonic and phasic pupillary components under different sustained cognitive load conditions? b) What is the relationship between tonic and phasic pupil response during sustained cognitive load?
Section snippets
Subjects
The subjects were 14 healthy volunteers (4 females, 2 left-handed, age 26.6 ± 5.0, educational level 15.9 ± 2.4), students and staff of ISAE-SUPAERO (French Aerospace Engineering School). All reported normal auditory acuity and normal or corrected-to-normal vision, had no history of neurological diseases and were free of the regular use of medication. The subjects slept 7.1 ± 1.1 h the night before the experiment and 8 out of 14 took coffee at least 2 h before the start of the experiment. All
Behavioral performance
The behavioral performance measures are presented in Fig. 2. The main effect of working memory load on accuracy was significant, F(1, 13) = 19.2, p < 0.001, partial η2 = 0.60, participants performing better at the 1-back task compared with the 2-back task. There were neither luminance, F(1, 13) = 1.2, p = 0.28, nor interaction effect on accuracy, F(1, 13) = 0.1, p = 0.83.
The main effect of working memory load on RT was also significant, F(1, 13) = 48.8, p < 0.001, partial η2 = 0.79, participants being faster to
Discussion
The goal of this study was to examine the impact of luminance on sustained and transient components of cognitive pupillary response – tonic pupil diameter and phasic pupil response – during sustained cognitive load. To that end, we designed a novel paradigm – Toulouse N-back Task – that allows a simultaneous study of both sustained and transient components of cognitive pupillary response. This working-memory task couples classic n-back task with mathematical problem-solving. The task induces
Conclusion
In the present study, we showed that the screen luminance has an impact on the cognitive pupillary reaction. It is an important issue, together with the impact of ambient illuminance, when performing pupillometric experiments in ecological conditions, and also when comparing results issued from different laboratories or setups. We dissociated tonic pupil diameter and phasic pupil response and showed that depending on the nature of the cognitive load – sustained or transient – the corresponding
References (39)
- et al.
Role of locus coeruleus in attention and behavioral flexibility
Biol. Psychiatry
(1999) - et al.
Effects of luminance and illuminance on visual fatigue and arousal during digital reading
Comput. Hum. Behav.
(2014) - et al.
Evidence for effects of task difficulty but not learning on neurophysiological variables associated with effort
Int. J. Psychophysiol.
(2014) - et al.
More than meets the eye: the relationship between pupil size and locus coeruleus activity
Neuron
(2016) - et al.
You can see pain in the eye: pupillometry as an index of pain intensity under different luminance conditions
Int. J. Psychophysiol.
(2008) - et al.
Relationships between pupil diameter and neuronal activity in the locus coeruleus, colliculi, and cingulate cortex
Neuron
(2016) - et al.
Frequency analysis of a task-evoked pupillary response: luminance-independent measure of mental effort
Int. J. Psychophysiol.
(2015) - et al.
Sympathetic and parasympathetic innervation of pupillary dilation during sustained processing
Int. J. Psychophysiol.
(2004) - et al.
A circuit for pupil orienting responses: implications for cognitive modulation of pupil size
Curr. Opin. Neurobiol.
(2015) - et al.
An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance
Annu. Rev. Neurosci.
(2005)
Locus coeruleus: from global projection system to adaptive regulation of behavior
Brain Res.
Task-evoked pupillary responses, processing load, and the structure of processing resources
Psychol. Bull.
Phasic not tonic pupillary responses vary with auditory vigilance performance
Psychophysiology
Background light intensity and the pupillary response in a reaction time task
Psychon. Sci.
Eliciting Sustained Mental Effort Using the Toulouse N-Back Task: Prefrontal Cortex and Pupillary Responses
Temporal dynamics of brain activation during a working memory task
Nature
Decision-related pupil dilation reflects upcoming choice and individual bias
Proc. Natl. Acad. Sci.
Pupil diameter tracks changes in control state predicted by the adaptive gain theory of locus coeruleus function
Cogn. Affect. Behav. Neurosci.
Pupil size in relation to mental activity during simple problem-solving
Science
Cited by (47)
Alerting effects require the absence of surprise
2024, Acta PsychologicaEffect of recurrent task-induced acute stress on task performance, vagally mediated heart rate variability, and task-evoked pupil response
2024, International Journal of PsychophysiologyCognitive characteristics in firefighter wayfinding Tasks: An Eye-Tracking analysis
2022, Advanced Engineering InformaticsAcute exercise effects on inhibitory control and the pupillary response in young adults
2021, International Journal of PsychophysiologyCitation Excerpt :Such a pupillary light response could be avoided by, instead, using black stimuli on a gray background to reduce the visual contrast, which has been found efficacious in reducing the pupillary light response in previous pupillometric studies with inhibitory control tasks (van Steenbergen and Band, 2013; van Steenbergen et al., 2015). Interestingly, other research has shown that a gray background (lower contrast/luminance) modulates tonic pupil dilation under higher cognitive load compared to black stimuli presented on a white background (higher contrast/luminance), while phasic dilation remained unaffected by higher cognitive load conditions (Peysakhovich et al., 2016). As such, the question remains whether utilizing a different stimulus environment (i.e., gray and black color contrasts) may afford adequate pupil modulation following exercise intervention.