Neural correlates of fast pupil dilation in nonhuman primates: Relation to behavioral performance and cognitive workload

Pupil dilation in humans has been previously shown to correlate with cognitive workload, whereby increased frequency of dilation is associated with increased degree of difficulty of a task. It has been suggested that frontal oculomotor brain areas control cognitively related pupil dilations, but this has not been confirmed due to lack of animal models of cognitive workload and task-related pupil dilation. This is the first report of a wavelet analysis applied to continuous measures of pupil size used to detect the onset of abrupt pupil dilations and the frequency of those dilations in nonhuman primates (NHPs) performing a trial-unique delayed-match-to-sample (DMS) task. A unique finding shows that electrophysiological recordings in the same animals revealed firing of neurons in frontal cortex correlated to different components of pupil dilation during task performance. It is further demonstrated that the frequency of fast pupil dilations (but not rate of eye movements) correlated with cognitive workload during task performance. Such correlations suggest that frontal neuron encoding of pupil dilation provides critical feedback to other brain areas involved in the processing of complex visual information.

[1]  Robert E Hampson,et al.  Systemic and Nasal Delivery of Orexin-A (Hypocretin-1) Reduces the Effects of Sleep Deprivation on Cognitive Performance in Nonhuman Primates , 2007, The Journal of Neuroscience.

[2]  A. Toga,et al.  The Rhesus Monkey Brain in Stereotaxic Coordinates , 1999 .

[3]  Gustavo Deco,et al.  Attention in natural scenes: Neurophysiological and computational bases , 2006, Neural Networks.

[4]  Attentional blink modulation during sustained and after discrete lead stimuli presented in three sensory modalities. , 2003, Psychophysiology.

[5]  Jun Tanji,et al.  Distribution of eye- and arm-movement-related neuronal activity in the SEF and in the SMA and Pre-SMA of monkeys. , 2002, Journal of neurophysiology.

[6]  Robert E Hampson,et al.  Facilitation of Task Performance and Removal of the Effects of Sleep Deprivation by an Ampakine (CX717) in Nonhuman Primates , 2005, PLoS biology.

[7]  N. P. Bichot,et al.  Effects of similarity and history on neural mechanisms of visual selection , 1999, Nature Neuroscience.

[8]  Anton van Boxtel,et al.  Differences in autonomic physiological responses between good and poor inductive reasoners , 2001, Biological Psychology.

[9]  Linda J. Lanyon,et al.  A model of active visual search with object-based attention guiding scan paths , 2004, Neural Networks.

[10]  Parashkev Nachev,et al.  Role of the human supplementary eye field in the control of saccadic eye movements , 2007, Neuropsychologia.

[11]  S. Funahashi.  Prefrontal cortex and working memory processes , 2006, Neuroscience.

[12]  David L Neumann,et al.  Attentional blink reflex modulation in a continuous performance task is modality specific. , 2004, Psychophysiology.

[13]  Daniel J. Buysse,et al.  Relationships between affect, vigilance, and sleepiness following sleep deprivation , 2008, Journal of sleep research.

[14]  N. P. Bichot,et al.  Continuous processing in macaque frontal cortex during visual search , 2001, Neuropsychologia.

[15]  E. Granholm,et al.  Pupillary responses index cognitive resource limitations. , 1996, Psychophysiology.

[16]  Marcel Adam Just,et al.  An fMRI Study of Bilingual Sentence Comprehension and Workload , 2002, NeuroImage.

[17]  T. Jung,et al.  Combined eye activity measures accurately estimate changes in sustained visual task performance , 2000, Biological Psychology.

[18]  I. G. Sil’kis.  The contribution of synaptic plasticity in the basal ganglia to the processing of visual information , 2007, Neuroscience and Behavioral Physiology.

[19]  T. Troscianko,et al.  Effort during visual search and counting: Insights from pupillometry , 2007, Quarterly journal of experimental psychology.

[20]  J. Jolles,et al.  Pupil dilation in response preparation. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[21]  J. Rodd,et al.  Processing Objects at Different Levels of Specificity , 2004, Journal of Cognitive Neuroscience.

[22]  Edward L Keller,et al.  Neural Activity in the Frontal Eye Fields Modulated by the Number of Alternatives in Target Choice , 2008, The Journal of Neuroscience.

[23]  Heiko Neumann,et al.  A neural model of feature attention in motion perception , 2007, Biosyst..

[24]  A. Nuthmann,et al.  Picture-word matching: flexibility in conceptual memory and pupillary responses. , 2003, Psychophysiology.

[25]  J. L. Kenemans,et al.  Visual stimulus change and the orienting reaction: event-related potential evidence for a two-stage process , 1992, Biological Psychology.

[26]  Liang-Shih Fan,et al.  Electrical capacitance tomography imaging of gas-solid and gas-liquid-solid fluidized bed systems , 2004, J. Vis..

[27]  David A. Kobus,et al.  Overview of the DARPA Augmented Cognition Technical Integration Experiment , 2004, Int. J. Hum. Comput. Interact..

[28]  M. Just,et al.  The intensity dimension of thought: pupillometric indices of sentence processing. , 1993, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[29]  J. Tanji.  The supplementary motor area in the cerebral cortex , 1994, Neuroscience Research.

[30]  Erik D. Reichle,et al.  From the Selectedworks of Marcel Adam Just Working Memory and Executive Function: Evidence from Neuroimaging Classic Issues Neuroimaging Results Working Memory and Executive Function: Evidence from Neuroimaging Reconstruals Suggested by the Neuroimaging Data Collaboration and Redundancy , 2022 .

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

[32]  C. Koch,et al.  Probabilistic modeling of eye movement data during conjunction search via feature-based attention. , 2007, Journal of vision.

[33]  Ottmar V. Lipp,et al.  Spontaneous and reflexive eye activity measures of mental workload , 2002 .

[34]  C. Bruce,et al.  Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. , 1985, Journal of neurophysiology.

[35]  J Hyönä,et al.  Pupil Dilation as a Measure of Processing Load in Simultaneous Interpretation and Other Language Tasks , 1995, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[36]  Scott Makeig,et al.  Eye Activity Correlates of Workload during a Visuospatial Memory Task , 2001, Hum. Factors.

[37]  J. Schall,et al.  Neuronal activity related to visually guided saccadic eye movements in the supplementary motor area of rhesus monkeys. , 1991, Journal of neurophysiology.

[38]  D. Ballard,et al.  Eye movements in natural behavior , 2005, Trends in Cognitive Sciences.

[39]  P. Vermersch,et al.  Pupillary disturbances in multiple sclerosis: correlation with MRI findings , 2001, Journal of the Neurological Sciences.

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

[41]  Sandra P Marshall,et al.  Identifying cognitive state from eye metrics. , 2007, Aviation, space, and environmental medicine.

[42]  E. Granholm,et al.  Pupillary responses on the visual backward masking task reflect general cognitive ability. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[43]  Stefan Treue,et al.  Attending to Features inside and outside the Spotlight of Attention , 2007, Neuron.

[44]  Terrence R Stanford,et al.  Categorization in the monkey hippocampus: a possible mechanism for encoding information into memory. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Hiroshi Shibasaki,et al.  Human eye fields in the frontal lobe as studied by epicortical recording of movement-related cortical potentials. , 2004, Brain : a journal of neurology.

[46]  C. Koch,et al.  Pupil dilation reflects perceptual selection and predicts subsequent stability in perceptual rivalry , 2008, Proceedings of the National Academy of Sciences.

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

[48]  E. Granholm,et al.  Culture-Fair Cognitive Ability Assessment , 2005, Assessment.

[49]  Peter A. Cariani,et al.  Temporal codes and computations for sensory representation and scene analysis , 2004, IEEE Transactions on Neural Networks.