Changes in pupil diameter entrained by cortically initiated changes in attention LORI B. DANIELS, 1 DAVID F. NICHOLS, 2 MATHEW S. SEIFERT, 1 AND HOWARD S. HOCK 1,3 1 Department of Psychology, Florida Atlantic University, Boca Raton, Florida 2 Department of Psychology, Roanoke College, Salem, Virginia 3 Center for Complex Systems and Brain Sciences, Florida Atlantic University, Boca Raton, Florida (RECEIVED August 18, 2011; ACCEPTED December 10, 2011) Abstract The diameter of the pupil is affected by changes in ambient illumination, color, spatial structure, movement, and mental effort. It has now been found that pupil diameter can be affected by cognitive processes. That is, it can be entrained by alternations between broadly spread and narrowly focused attention that are cued exogenously (attention is “summoned” by the cue) or endogenously (attention changes under the perceiver’s intentional control). Pupil diameter also is affected by post-eye-blink constrictions that occur most often when attention is narrowed, and possibly by changes evoked by the near reflex, although changes in attention state parsimoniously account for the entirety of the results. Changes in pupil diameter produce differences in spherical aberration that alternately blur (when the pupil dilates) and sharpen the retinal image (when the pupil constricts), affecting the relative sensitivity of large receptive fields that mediate broadly spread attention compared with smaller receptive fields that mediate more narrowly focused attention. Results for endogenously cued, intentional changes in attentional spread provide definitive behavioral evidence for cortical feedback to subcortical nuclei that control pupil diameter, either directly or through pupil-constricting eye blinks. Analyses of convergent and divergent changes in eye position indicate that the near reflex was activated long after the initiation of relatively gradual attentionally cued changes in pupil diameter, and further, that when it occurs, the near reflex facilitates ongoing changes in pupil diameter. Keywords: Pupil dynamics, Attentional spread, Cortical feedback, Spherical aberration Introduction It has long been known that the diameter of the pupil changes in response to changes in ambient illumination, the purpose being to control the brightness of the light falling on the retina. However, the pupil also responds to changes in color, spatial structure, and movement (Slooter & van Norren, 1980; Young & Alpern, 1980; Young et al., 1993; Young & Kennish, 1993; Sahraie & Barbur, 1997; Gamlin et al., 1998). In addition, it is well known that internal states entailing arousal, effort, interest, and emotion are observable through their effect on the diameter of the pupil (Hess & Polt, 1960; Kahneman & Beatty, 1966; Beatty, 1982). In the experiments reported in this article, it is determined whether the diameter of the pupil can be affected by cognitive mechanisms entailing changes in attention, irrespective of differences in mental effort. More specifically, we investigate whether the di- ameter of the pupil can be entrained by alternations between broadly spread and narrowly focused attention. If it were found that pupil dilation is greater for broad than narrow attention, it would provide evidence that differences in spherical aberration are associated with the alternating attentional states. That is, greater spherical aberration when the pupil is dilated would blur the retinal image, decreasing the contrast of high spatial frequency information (Campbell & Green, 1965; Campbell & Gubish, 1966), and thereby, increasing the relative sensitivity of the large receptive fields that mediate broadly spread attention compared with the smaller receptive fields that mediate more narrowly focused attention (Hock & Balz, 1994; Balz & Hock, 1997; Hock et al., 1998; Hochstein & Ahissar, 2002). It is determined whether pupil-entraining changes in attentional spread can be cued both exogenously (attention elicited by the stimulus) and endoge- nously (attention controlled by the perceiver) (Jonides, 1981; Corbetta & Shulman, 2002). It also is determined whether differences in pupil diameter can result from sustained broad attention compared with sustained narrow attention. When endogenously cued, changes in attentional spread are intentional, so they must be initiated cortically. Evidence for pupil entrainment with endogenous cueing therefore would provide strong behavioral support for cortical feedback influencing the subcortical control of pupil diameter (Gamlin et al., 1998; Barbur, 2004). Materials and methods The diameter of the pupil is notoriously variable, even in the absence of stimulation, so differences between broadly spread and narrowly focused attention could not be consistently observed by the examination of pupillary time series. To address this problem, the two attentional states were rhythmically alternated, and the Address correspondence and reprint requests to: Howard S. Hock, Department of Psychology, Florida Atlantic University, Boca Raton, FL, 33431. E-mail: hockhs@fau.edu 1 Visual Neuroscience (2012), 0, Page 1 of 12. Copyright Ó Cambridge University Press, 2012 0952-5238/12 $25.00 doi:10.1017/S0952523812000077