A circuit for pupil orienting responses: implications for cognitive modulation of pupil size
Introduction
Efficient visual coding begins in the eye. Light enters the eye through, and is controlled by, the pupil. The pupil constricts in response to an increase of global luminance level, which is typically referred to as the pupillary light reflex, and it dilates for a global luminance decrease, referred to as the darkness reflex [1]. The quality of the signal projected on the retina is already under the control of this simple mechanism. This illumination-dependent pupil modulation is well understood, and thought to regulate the trade-off between sensitivity and sharpness for the optimization of image quality [2, 3]. Additionally, pupil dilation has been linked to various cognitive processes [4], which we refer to as cognition-related pupil responses. Over the past decade, a growing body of research has used pupil size to investigate various cognitive processes, demonstrating correlations between pupil size and aspects in cognition such as target detection, perception, learning, memory, and decision making (e.g. [5, 6, 7, 8, 9, 10, 11, 12]).
Changes in pupil size have also been associated with the orienting response [13, 14], we refer to these responses as orienting-related pupil responses. The presentation of a salient stimulus initiates a series of responses to orient the body for appropriate action, including not only saccades and attentional shifts [15, 16], but also transient pupil dilation [1, 17•, 18••, 19•]. The function of this pupil dilation is thought to increase visual sensitivity [13], although empirical evidence to support the argument is lacking [20]. The superior colliculus (SC; optic tectum in non-mammals), one of most important structures related to saccadic eye movements and spatial attention [21, 22••], may also play a central role in coordinating this orienting-related pupil response [17•, 18••, 23, 24••], highlighting a novel neural substrate to possibly coordinate various cognitive processes and pupil diameter. Here, we review the evidence supporting the link of the SC to orienting-related pupil responses, focusing on recent work in monkeys and humans.
Section snippets
Pupil control circuit
Pupil size is controlled by the balanced activity between sympathetic and parasympathetic pathways (Figure 1) that have been identified and reviewed in detail elsewhere [1, 25]. Briefly, in the parasympathetic system, retinal ganglion cells project directly to the pretectal olivary nucleus (PON), which in turn projects bilaterally to the Edinger–Westphal (EW) nucleus [26]. Preganglionic parasympathetic neurons in the EW project to the ciliary ganglion to control pupillary constriction muscles
Pupil responses to salient stimuli
Numerous studies have identified a significant effect of stimulus saliency on shifts of gaze and attention [15, 16], but saliency effects on the orienting-related pupil response are less understood. Stimulus contrast is one of the most primitive saliency components [49], and has been implemented as a component of saliency in a number of computational models [50]. Changing the contrast of a target has dramatic effects on sensory responses in the SCi and ensuing saccadic reaction times (SRT),
Pupil responses to multisensory stimuli
Salient visual and auditory stimuli, when presented alone, elicit transient pupil dilation. This raises an intriguing question of how salient signals from the different modalities (i.e., visual and auditory) are combined to influence pupil dynamics. One hallmark of SCi processing is multisensory integration [55]. If the orienting-related pupil responses are coordinated by the SCi, salient stimuli presented from different modalities should be integrated in the SCi to produce coordinated pupil
Pupil responses to SC microstimulation
Although the central role of the SCi on shifts of gaze and attention is well-established [21, 22••], its role is less clear on other components of orienting such as pupil dilation. SCi microstimulation evokes saccades and deactivation of the SCi interrupts saccades toward the affected location of the visual field [21]. Studies exploring SCi microstimulation on the shift of attention demonstrate facilitative effects for stimuli presented in the stimulated location of the visual field and neurons
Modulation of pupil responses by saccade preparation
Pupil responses are also modulated by top-down processes [4], and some of these modulations may be associated with SC-mediated pupil pathways. The anti-saccade task is frequently used to examine voluntary control because subjects are instructed prior to stimulus appearance to either generate a pro-saccade (look at a peripheral stimulus) or an anti-saccade (look in the opposite direction of the stimulus). Unlike the automatic visuomotor response required in the pro-saccade condition, to complete
Conclusions and clinical applications
The orienting-related pupil response has the potential to be used as a biomarker for clinical investigation because of the proposed link of top-down processes in the frontoparietal cortex and basal ganglia to the pupil control circuit via the SCi (Figure 1). We propose that dysfunction in the fronto-parietal cortex and basal ganglia can lead to altered pupil responses in cognitive tasks. For example, the ability to recognize stimulus saliency is impaired among patients with neurological
Conflict of interest statement
Nothing declared.
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
This work was supported by Canadian Institutes of Health Research Grant (MOP-136972). D.P.M. was supported by the Canada Research Chair Program.
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