The impact of luminance on tonic and phasic pupillary responses to sustained cognitive load.

Pupillary reactions independent of light conditions have been linked to cognition for a long time. However, the light conditions can impact the cognitive pupillary reaction. Previous studies underlined the impact of luminance on pupillary reaction, but it is still unclear how luminance modulates the sustained and transient components of pupillary reaction - tonic pupil diameter and phasic pupil response. In the present study, we investigated the impact of the luminance on these two components under sustained cognitive load. Fourteen participants performed a novel working memory task combining mathematical computations with a classic n-back task. We studied both tonic pupil diameter and phasic pupil response under low (1-back) and high (2-back) working memory load and two luminance levels (gray and white). We found that the impact of working memory load on the tonic pupil diameter was modulated by the level of luminance, the increase in tonic pupil diameter with the load being larger under lower luminance. In contrast, the smaller phasic pupil response found under high load remained unaffected by luminance. These results showed that luminance impacts the cognitive pupillary reaction - tonic pupil diameter (phasic pupil response) being modulated under sustained (respectively, transient) cognitive load. These findings also support the relationship between the locus-coeruleus system, presumably functioning in two firing modes - tonic and phasic - and the pupil diameter. We suggest that the tonic pupil diameter tracks the tonic activity of the locus-coeruleus while phasic pupil response reflects its phasic activity. Besides, the designed novel cognitive paradigm allows the simultaneous manipulation of sustained and transient components of the cognitive load and is useful for dissociating the effects on the tonic pupil diameter and phasic pupil response.

[1]  Brian D Corneil,et al.  Transient Pupil Dilation after Subsaccadic Microstimulation of Primate Frontal Eye Fields , 2016, The Journal of Neuroscience.

[2]  J. Beatty,et al.  Phasic not tonic pupillary responses vary with auditory vigilance performance. , 1982, Psychophysiology.

[3]  D Kahneman,et al.  Pupil Diameter and Load on Memory , 1966, Science.

[4]  T. Knapen,et al.  Decision-related pupil dilation reflects upcoming choice and individual bias , 2014, Proceedings of the National Academy of Sciences.

[5]  J. Beatty.  Task-evoked pupillary responses, processing load, and the structure of processing resources. , 1982, Psychological bulletin.

[6]  S. Steinhauer,et al.  Sympathetic and parasympathetic innervation of pupillary dilation during sustained processing. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[7]  J. Lacey,et al.  THE EVALUATION OF AUTONOMIC RESPONSES: TOWARD A GENERAL SOLUTION , 1956, Annals of the New York Academy of Sciences.

[8]  E. N. Sokolov,et al.  Perception and the Conditioned Reflex , 1965 .

[9]  W. Dewhurst.  Stimulus and response—The law of initial value , 1968 .

[10]  M. Causse,et al.  Eliciting Sustained Mental Effort Using the Toulouse N-Back Task: Prefrontal Cortex and Pupillary Responses , 2017 .

[11]  Albrecht Schmidt,et al.  A Model Relating Pupil Diameter to Mental Workload and Lighting Conditions , 2016, CHI.

[12]  Mickaël Causse,et al.  Neural and psychophysiological correlates of human performance under stress and high mental workload , 2016, Biological Psychology.

[13]  Edward E. Smith,et al.  Temporal dynamics of brain activation during a working memory task , 1997, Nature.

[14]  Mickaël Causse,et al.  Frequency analysis of a task-evoked pupillary response: Luminance-independent measure of mental effort. , 2015, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[15]  E. Szabadi,et al.  Functional Neuroanatomy of the Noradrenergic Locus Coeruleus: Its Roles in the Regulation of Arousal and Autonomic Function Part II: Physiological and Pharmacological Manipulations and Pathological Alterations of Locus Coeruleus Activity in Humans , 2008, Current neuropharmacology.

[16]  R. O’Connell,et al.  Pupillometry and P3 index the locus coeruleus-noradrenergic arousal function in humans. , 2011, Psychophysiology.

[17]  R. Barry,et al.  Pupillary responses and event-related potentials as indices of the orienting reflex. , 2011, Psychophysiology.

[18]  T. Areta.  [Sympathetic and parasympathetic]. , 1960, Anais paulistas de medicina e cirurgia.

[19]  Jan Theeuwes,et al.  Cognitive and Ocular Factors Jointly Determine Pupil Responses under Equiluminance , 2016, PloS one.

[20]  Paul Pauli,et al.  You can see pain in the eye: pupillometry as an index of pain intensity under different luminance conditions. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[21]  Jonathan D. Cohen,et al.  An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. , 2005, Annual review of neuroscience.

[22]  Mark S. Gilzenrat,et al.  Pupil diameter tracks changes in control state predicted by the adaptive gain theory of locus coeruleus function , 2010, Cognitive, affective & behavioral neuroscience.

[23]  J. Bradshaw.  Background light intensity and the pupillary response in a reaction time task , 1969 .

[24]  E. Szabadi,et al.  Functional Neuroanatomy of the Noradrenergic Locus Coeruleus: Its Roles in the Regulation of Arousal and Autonomic Function Part I: Principles of Functional Organisation , 2008, Current neuropharmacology.

[25]  R. O’Connell,et al.  Pupil diameter covaries with BOLD activity in human locus coeruleus , 2014, Human brain mapping.

[26]  D. Whitaker,et al.  Factors affecting light-adapted pupil size in normal human subjects. , 1994, Investigative ophthalmology & visual science.

[27]  P. Jin,et al.  Toward a reconceptualization of the law of initial value. , 1992, Psychological bulletin.

[28]  D. Kahneman.  Pupillary Responses in a Pitch-Discrimination Task , 1967 .

[29]  J. Wilder,et al.  Stimulus and Response: the Law of Initial Value , 2014 .

[30]  Thierry Baccino,et al.  Effects of luminance and illuminance on visual fatigue and arousal during digital reading , 2014, Comput. Hum. Behav..

[31]  E. Hess,et al.  Pupil Size in Relation to Mental Activity during Simple Problem-Solving , 1964, Science.

[32]  Jonathan D. Cohen,et al.  Role of locus coeruleus in attention and behavioral flexibility , 1999, Biological Psychiatry.

[33]  Vincent D Costa,et al.  More than Meets the Eye: the Relationship between Pupil Size and Locus Coeruleus Activity , 2016, Neuron.

[34]  G. Aston-Jones,et al.  Locus coeruleus: From global projection system to adaptive regulation of behavior , 2016, Brain Research.

[35]  J. Beatty,et al.  Pupillary responses in a pitch-discrimination task , 1967 .

[36]  F. Paas,et al.  Memory load and the cognitive pupillary response in aging. , 2004, Psychophysiology.

[37]  Douglas P Munoz,et al.  A circuit for pupil orienting responses: implications for cognitive modulation of pupil size , 2015, Current Opinion in Neurobiology.

[38]  Jeremy R. Reynolds,et al.  Distinct neural circuits support transient and sustained processes in prospective memory and working memory. , 2009, Cerebral cortex.

[39]  W W Tryon,et al.  Pupillometry: a survey of sources of variation. , 1975, Psychophysiology.

[40]  H. Lüdtke,et al.  The effect of caffeine on spontaneous pupillary oscillations , 2014, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[41]  Jan B. F. van Erp,et al.  Evidence for effects of task difficulty but not learning on neurophysiological variables associated with effort. , 2014, International Journal of Psychophysiology.

[42]  J. Gold,et al.  Relationships between Pupil Diameter and Neuronal Activity in the Locus Coeruleus, Colliculi, and Cingulate Cortex , 2016, Neuron.