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PUPILLARY RESPONSES, COGNITIVE PSYCHOPHYSIOLOGY AND PSYCHOPATHOLOGY

Stuart R. Steinhauer, Ph.D.
Research Associate Professor of Psychiatry, University of Pittsburgh School of Medicine

Mailing Address: Biometrics Research, 151R
Department of Veterans Affairs Medical Center
7180 Highland Drive, 
Pittsburgh, PA 15206 USA
Tel. 412-365-5251    FAX  412-365-5259    Email: sthauer@ pitt.edu

Contents
I. Introduction
II. General Background and Historical Perspective
III. Cognitive Psychophysiology and Pupillography: 
Psychophysiological Measurement of Processing Effort, Capacity, and Information.  
IV.  Psychopathology and Pupillary Motility
V. References

I. Introduction

            This section has two objectives: 1) to provide a brief overview of the pupillary response in relation to cognitive processes in normal and abnormal populations, and 2) to provide an update of papers during the past decade that have not been reviewed in summary papers.  The reference list includes papers published from 1990 onward; not all of these papers are summarized in the review.

            The following sections briefly review findings for components of information processing as reflected in the human pupillary response, and the relation of these measures to psychological phenomena in normal and neuropsychiatric patient groups.  Both the constriction of the pupil to light (miosis), as well as the dilation (dilatation; mydriasis) resulting from information delivery, have provided useful adjuncts in the study of psychopathology, especially with reference to schizophrenia.  Following summaries of some of the seminal findings, more recent papers are referenced.  (Papers dealing with sensory reactions, or neurological reactivity unrelated to cognitive activation, are not usually included in this overview or the reference section).

            Review Papers: Previous journal or book chapters which review pupillary data in relation to psychology include a brief paper by Tryon (1975), Goldwater (1982), Hakerem (1967), Hess (1972; 1975; 1987), and Beatty (1982 ;1986; Beatty and Wagoner, 2000),. 

            Books: Janisse (1974) published the proceedings of the Manitoba Pupil symposium of 1973, with relevant chapters by Hakerem, Peavler, Hess and Goodwin, Bernick, and Rubin.  Books dealing with the psychology of the pupillary response have been published by Hess (1975), Janisse (1977), and Loewenfeld (1993; see chapters 14 and 45, respectively, dealing with psychology and psychiatry).   A particularly good recent overview has been provided by Andreassi (2000).

            A review of pupillary reactions in schizophrenia was provided by Zahn, Frith, & Steinhauer (1991), following earlier reviews of psychophysiology and psychopathology by Spohn and Patterson (1979) and Zahn (1986).  Much of the following review is adapted from Steinhauer and Hakerem (1992).  More recent findings related to relatives of schizophrenic subjects have been summarized by Steinhauer and Friedman (1995).

            Integrative findings on pupillography have been presented at the International Colloquia on the Pupil, beginning in 1963.  The most recent meeting was held at Asilimar, California in September, 2001.  The next meeting will be held in Crete in 2003.  For details, and information  on Pupillary studies, see the Pupil page of Peter Howarth http://www.jiscmail.ac.uk/files/PUPIL/.

                        II. General Background and Historical Perspective

For centuries, the pupillary aperture has been thought of as a figurative window to the mind; with the advancement of medical sciences, the pupil began to serve as a literal window on brain function.  In her 1958 dissertation paper dealing primarily with pupillary dilatation, Loewenfeld (1958) cited nearly 1600 references, including 114 dated prior to 1830; her 1993 book lists over 15,000 references, covering up to about 1985. 

     Incidental observations of pupillary dilation associated with increased interest or arousal were well known, such as the use of belladonna to enlarge the pupil artificially as a cosmetic effect, and wearing of eyeshades to obscure any sudden dilatation for the poker player who might otherwise give away his hand.

The re-emergence of pupillary studies among psychologists is related to a series of reports from several different laboratories in the early 1960s in the areas of experimental psychology and experimental psychopathology.  The most polemic approach was generated by the initial papers of Eckhard Hess claiming pupillary dilation to positive affect stimuli and constriction to negative affect (Hess & Polt, 1960), which led to continuing controversies.  Sokolov (1963) emphasized the contributions of pupillary changes in defining the orienting reaction to novel environmental stimuli.  Hess and Polt also began to report on pupillary dilation during mental activities (Hess & Polt, 1964).  More carefully conducted studies began to appear involving threshold discrimination (Hakerem & Sutton, 1966), and work by Kahneman and colleagues (e.g., Kahneman & Beatty, 1966) represented a much stronger commitment to the developing concepts of cognitive psychology.

III. Cognitive Psychophysiology and Pupillography:

Psychophysiological Measurement of Processing Effort, Capacity, and Information.  Among those measures for which a correlate of both attentional effort and processing activities have been studied, perhaps the most widely emphasized is the pupillary dilation response (Beatty, 1982; Beatty, 1986; Goldwater, 1972; Janisse, 1977). Pupil diameter enlarges with increasing effort during performance.  This can be observed for purely mechanical effort, as when varying weights are picked up (Nunnally, Knott, Duchnowski, & Parker, 1967) or even when a simple finger press occurs, in which both response preparation and execution contribute to the dilation (Richer, Silverman, & Beatty, 1983).   Mental effort has been manipulated by a number of means, including arithmetic problems of varying difficulty (often a typical "mental stress" paradigm), language-based tasks (including reading of material forward and backwards; Metalis, Rhoades, Hess, & Petrovich, 1980), and especially the effect of increasing memory load during the digit span task, in which pupil diameter increases as the number of digits stored is increased (Kahneman & Beatty, 1966).  Of special interest is that as maximum effective storage (judged by performance) is reached, pupillary dilation reaches a maximum (Peavler, 1974).  When memory is overloaded, the pupil may even decrease in diameter, suggesting that it is sensitive to both the extent of processing capacity as well as the breakdown of capacity (Poock, 1973; Granholm et al., 1996).  Kahneman (1973) relied heavily on results from pupillary experiments in the development of his treatise dealing with basic components of attention and effort.  More recent approaches to information processing models such as neural networks have also ustilized pupillary data (Siegle, 1999a).

Pupillary dilation can also be evoked by tasks in which there is little effort employed in recognizing a stimulus, but for which the "informational value" of the stimulus is high.  Thus, simple click patterns show a quick habituation when the subject knows what each subsequent stimulus will be, but a clear dilation occurs to the clicks when the subject is asked to guess what stimulus pattern will occur (Hakerem, 1974).  Moreover, when the subject is not certain whether a click will actually occur at a specific point in time, but the absence of a click indicates a particular outcome (e.g., correct or incorrect, different amounts of monetary payoff), the "absence" of the stimulus itself elicits a pupillary dilation (Levine, 1969) which is related to the information conveyed by the stimulus absence.  Friedman et al. (1973) observed that the amplitudes of pupillary dilation and the amplitude of the P300 component of the event-related brain potential were inversely related to the subjective probabilities (an interaction of the subject's guessing behavior and the stimulus probabilities).  Thus, larger amplitudes were seen for the least likely events.  The same paradigm was employed by Bock (1976), who recorded pupillary and ERP data from monozygotic and dizygotic twin pairs, and from non-twin siblings.

In dealing with the complexities of stimulus qualities which affect pupil diameter, it is worthwhile to take a brief look at one of the major controversies in pupillary research -- the statements of Hess and colleagues (Hess & Polt, 1960; Hess, 1964) that positive affect is associated with dilation, while negative affect results in constriction.  Though the notion of constriction to aversive stimuli has been widely rejected, responses to arousing viusal stimuli continue to be studied (Aboyoun & Dabbs, 1998; Dabbs, 1997).  There have been many critical reviews of this research (e.g., Janisse, 1977), as well as attempts by Hess and his students to justify the work (Hess, Beaver, & Shrout, 1975).  Two of the problems involved in using complex visual stimuli, which have usually been overlooked, will be mentioned.

The first consideration involves so-called control slides, which are typically presented before each stimulus slide. The notion in several studies was that the control and stimulus slides should be matched for brightness, so that no differential constriction to the slides could occur, and differences could only be attributable to the content of the target stimulus slide. This approach, however, takes a naive view of the physiology of the optic system, including the afferent pathway even at the level of the retina.  When stimuli of either different wavelengths or different intensities strike similar regions of the retina, they differentially stimulate receptors, which evoke pupillary constrictions.  This was exquisitely demonstrated over two decades ago by Kohn and Clynes (1969): even matching for overall brightness did not eliminate sensory-related constrictions to the onset of different hues.

A second source of confounding is related to the pupillary constriction produced by the initial presentation of stimuli.  This portion of the response was usually ignored by researchers employing pictures, who looked at average diameters over periods as long as ten seconds, rather than the specific dynamic responses to the pictures used.  One exception to this was a study by Libby, Lacey and Lacey (1973), whose data clearly showed the initial constriction resulting from stimulus presentations.  In their study, pupillary dilation was most often seen to interesting pictures, and the unpleasant stimuli overall yielded larger dilations than pleasant stimuli -- a finding totally at odds with the Hess formulation.  Similarly, Steinhauer et al. (1983) examined the responses to a series of pictures varying in emotional content, but covaried out effects of initial diameter and the constriction produced by slide onset: the largest dilations were evoked by stimuli reported as most aversive or most pleasant, with smaller dilations to mildly unpleasant or pleasant stimuli, and the least dilation to neutral pictures.  Thus, the best controlled studies indicate that the level of emotional stimulation or interest, regardless of valence, is related to the pupillary dilation response, but the confounding effect of initial physiological reactions to visual stimuli must be carefully eliminated.

Genetic Contributions: One of the more intriguing aspects of psychophysiological data is that there is clear evidence that familial similarity can be observed in tonic activity as well as in time-varying measures of cognitive activity (Boomsma & Gabrielli, 1985).  Patterns of pupillary dilation have been examined among twin pairs in two dissertations conducted by students of Hakerem.  Bock (1976) compared pupillary dilation in identical twins, fraternal twins, and non-twin siblings during a guessing task.  Both objective numerical analyses of similarity, as well as judges' blind matching of pairs, indicated greater similarity of the pupil and ERP data for identical twins than for fraternal twins or non-twin siblings.  A more recent dissertation (Gaudreau, 1991) used a forced-choice procedure for matching pupillary waveforms, demonstrating significantly high rates of matching identical twin pairs across two different tasks.

Additional work has been conducted to examine underlying substrates of cognitive performance and pupillary reactions.  Beatty (1989) demonstrated that the pupil could respond with extremely small average dilations (.001 mm) to stimuli occurring at up to a rate of 3/sec.   Matthews et al. (1991) found that blockade of the sphincter by thymoxamine eliminated the dilation that was produced by an effortful task.  Granholm et al. (1996) reexamined the use of processing load, presenting subjects with 5, 9 or 13 digits during a digit span task.  As expected, processing load increased as demand increased, but more clearly showed stabilization when nearing maximum processing capacity, but decrease in pupil diameter once capacity was exceeded.

Language function has been examined using the pupil in studies of syntactic anomaly (Schluroff, 1982), lexical ambiguity (Ben-Nun, 1986), and syntactic complexity (Just and Carpenter, 1993).

Attempts to model the contributions of different sources contributing to pupillary movements have included bioengineering models (see the chapter by Stark in Loewenfeld's book).  Hoeks and Levelt (1992), and Hoeks and Ellenbroek (1993) have proposed a quantitative neural model, although they did not account for contributions of the sympathetic pathway to dilation processes.  Steinhauer has proposed a model in which sympathetic and parasympathetic components contribute differentially to dilation under varying task requirements, with different time courses for the contributions of the sympathetic and parasympathetic pathways (see Steinhauer and Hakerem, 1992). 

IV.  Psychopathology and Pupillary Motility

During the early years of this century, aberrations in pupillary responsivity were carefully noted in psychotic patients (cf. Hakerem & Lidsky, 1975; Hess, 1972), especially by German psychiatrists such as Bumke (1904) and Bach (1908), and were followed up with studies by Lowenstein and Westphal (1933), Levine and Schilder (1942), and May (1948) in the third and fourth decades.  Leonard Rubin, at Eastern Psychiatric Research Institute in Philadelphia, was employing pupillary measurement to develop hypotheses of autonomic imbalance in psychiatric patients (for an overview, see Rubin 1974).  While his attempts to define a variety of disorders based on the notions of central adrenergic and/or cholinergic activity as assessed by the pupil attracted some interest for a number of years, this conceptualization has been heavily criticized as being overly simplistic, and has been rejected by most researchers (see discussion by Loewenfeld, 1993).

Hakerem and colleagues at New York York State Psychiatric Institute conducted a number of initial studies which indicated decreased light reactions and abnormal response latencies in schizophrenics (Hakerem & Lidsky, 1969; Hakerem, Sutton, & Zubin, 1964; Lidsky, Hakerem, & Sutton, 1971), as well as difficulties in integrating irregular sequences of light pulses (Hakerem & Lidsky, 1975).  Decreased responsivity in schizophrenic patients for auditory and visual pupillary responses during cognitive tasks was reported by Steinhauer, Hakerem, and Spring (1979).

Steinhauer and Zubin (1982) reported decreased dilation, as well as decreased P300 amplitudes for schizophrenics compared to controls, during an auditory task in which infrequent stimuli normally evoke substantial pupillary dilation and P300 amplitudes.

Steinhauer et al. (1992) recorded the averaged light reaction in schizophrenic patients during neuroleptic treatment and subsequent (double-blind) drug free withdrawal.  Stabilization on haloperidol resulted in a significant increase in extent of constriction than during a subsequent drug-free period in patients.  Thus, neuroleptic treatment appeared to normalize the response slightly, but generally still kept the response measure below the mean for normals.  Data during the treatment phase were also found to predict likelihood of subsequent relapse.

There have been few additional studies of patients involving task-related dilation.  Straube (1982) reported that schizophrenics exhibited larger dilations than controls during performance of the digit span task, which could be interpreted as an indication that patients employed greater effort than did controls.  However, Granholm et al. (1996) reported decreased dilation in schizophrenic patients during the digit span task, a finding that appears to conflict with the report of Straube.  Morris et al. (1997) evaluated working memory using pupillary reactivity in schizophrenics.  Granholm et al. (1999) have used the pupillary response to probe semantic incongruities during verbal fluency in schizophrenic patients.

Several other types of patient groups have been studied.  Patients with toxic exposure to organic solvents exhibit reduced dilations during information processing tasks, but also show abnormal increases in overall diameter when even slightly more complex tasks are presented that are not difficult for normal subjects (Morrow & Steinhauer, 1995).  For alcoholic subjects, no differences between semantic and phonemic tasks have been observed (O'Leary et al., 1980).  An interesting series of studies by Bitsios and colleagues (1996, 1998a, 1998b) has employed the pupillary light reaction to probe the effects of anxiety and effectiveness of anxiolytics; the light reaction is reduced by anticipation of a fear-evoking event (Bitsios et al, 1996).  Patients with anxiety disorders, who show reduced light reactions (Bakes et al., 1990), show increasing light reaction amplitude when anxiolytics are administered (Bitsios et al., 1998).  Reduction of dilation to fearful stimuli during desensitization treatment of phobic patients has also been reported (Sturgeon et al, 1989).  Effects of rumination indicated by dilation have been examined among depressed patients (Siegle, 1999b).

 

References: Publications from 1990 on are marked by an asterisk

*Abouyon, D.C., & Dabbs, J.M., Jr. (1998). The Hess pupil dilation findings: Sex or novelty? Social Behavior & Personality, 26: 415-419.

*Andreassi, J.L. (2000).  Chap 10, Pupillary response and behavior. In: Psychophysiology: Human Behavior & Physiological Response.  Mahwah, N.J.:Lawrence Erlbaum Assoc., pp. 218-233.

Bach, L. (1908). Pupillenlehre. Anatomie, Physiologie und Pathologie. Methodik der Untersuching. Berlin: Karger.

*Backs, R.W., & Walrath, L.C. (1992). Eye movement and pupillary response indices of mental workload during visual search of symbolic displays. Applied Ergonomics, 23: 243-254.

Bakes, A., Bradshaw, C.M., & Szabadi, E. (1990). Attenuation of the pupillary light reflex in anxious patients. British Journal of Clinical Pharmacology, 30: 377-381.

Beatty, J. (1982). Task-evoked pupillary responses, processing load, and the structure of processing resources. Psychological Bulletin, 91: 276-292.

Beatty, J. (1986). The pupillary system. In G. H. Coles, E. Donchin, & S. W. Porges, (Eds.), Psychophysiology: Systems, Process, and Applications (pp. 43-50). New York: Guilford Press.

Beatty, J. (1989). Pupillometric signs of selective attention in man. In E. Donchin, G. Galbraith, & M.L. Kietzman, (Eds.), Neurophysiology and Psychology: Basic Mechanisms and Clinical Applications. New York: Academic Press, pp. 138-143.

*Bernhardt, P.C., Dabbs, J.M., & Riad, J.K. (1996). Pupillometry system of use in social psychology. Behavior Research Methods, Instruments, & Computers, 28: 61-66.

*Birnbaum, M.H., & Thomann, K. (1996). Visual function in multiple personality disorder. Journal of the American Optometric Association, 67: 327-334.

*Bitsios, P., Szabadi, E., Bradshaw, C.M., (1996). The inhibition of the pupillary light reflex by the threat of an electric shock: a potential laboratory model of human anxiety. Journal of Psychopharmacology, 10: 279-287.

*Bitsios, P., Szabadi, E., Bradshaw, C.M., (1998). The effects of clonidine on the fear-inhibited light reflex. Journal of Psychopharmacology, 12: 137-145.

*Bitsios, P., Szabadi, E., Bradshaw, C.M., (1998). Sensitivity of the fear-inhibited light reflex to diazepam. Psychopharmacology, 135: 93-98.

Bock, F. A. (1976). Pupillary dilation and vertex evoked potential similarity in monozygotic and dizygotic twins and siblings. (Doctoral dissertation, City University of New York, NY, 1976). Dissertation Abstracts International, 36, 6432B.

Boomsma, D. I., & Gabrielli, W. F., Jr. (1985).  Behavioral genetic approaches to psychophysiological data. Psychophysiology, 22: 249-260.

*Brown, G.G., Kindermann, S.S., Siegle, G.J., Granholm, E., Wong, E.C., & Buxton, R.B. (1999). Brain activation and pupil response during covert performance of the Stroop Color Word task. Journal of the International Neuropsychological Society, 5: 308-319.

Bumke, O. (1904). Die Pupillenstörungen, Bei Geistes -- und Nervenkrankheiten (Physiologie und Pathologie der Irisbewegungen). Jena: Fischer.

*Cassady, J.M. (1996). Increased firing of neurons in the posterior hypothalamus which precede classically conditioned pupillary dilations. Behavioral Brain Research, 80: 111-121.

Chaney, R.H., Linzmayer, L., Grunberger, M., & Saletu, B. (1989). Pupillary responses in recognizing awareness in persons with profound mental retardation. Perceptual & Motor Skills, 69: 523-528.

*Chapman, C.R., Oka, S., Bradshaw, D.H., Jacobson, R.C., & Donaldson, G.W. (1999). Phasic pupil dilation response to noxious stimulation in normal volunteers: Relationship to brain evoked potentials and pain report. Psychophysiology, 36: 44-52.

*Dabbs, J.M., Jr. (1997). Testosterone and pupillary response to auditory sexual stimuli. Physiology & Behavior, 62: 909-912.

*Deijen, J.B., van der Beeke, E.J., Orlebeke, J.F., & van den Berg, H. (1992). Vitamin B-6 supplementation in elderly men: Effects on mood, memory, performance and mental effort. Psychopharmacology, 109: 489-496.

*Deijen, J.B., Heemstra, M.L., & Orlebeke, J.F. (1995). Pupillometric assessment of compensatory effort in a memory search task under physical and pharmacologically-induced suboptimal states. Canadian Journal of Experimental Psychology, 49: 387-396.

*Deijen, J.B., Orlebeke, J.F., & Rijsdijk, F.V. (1993). Effect of depression on psychomotor skills, eye movements and recognition-memory. Journal of Affective Disorders, 29: 33-40.

*Ellermeier, W., & Westphal, W. (1995). Gender differences in pain ratings and pupil reactions to painful pressure stimuli. Pain, 61: 435-439.

*Fountoulakis, K, Fotiou, F, Iacovides, A., Tsiptsios, J. Golas, A., Tsolaki, M., & Ierodiakonou, C. (1999). Changes in pupil reaction to light in melancholic patients. International Journal of Psychophysiology, 31: 121-128.

Friedman, D., Hakerem, G., Sutton, S., & Fleiss, J. L. (1973). Effect of stimulus uncertainty on the pupillary dilation response and the vertex evoked potential. Electroencephalography and Clinical Neurophysiology, 34: 475-484.

*Garrett, J.C., Harrison, D.W., & Kell, P.L. (1989). Pupillometric assessment of arousal to sexual stimuli: Novelty effects or preference? Archives of Sexual Behavior, 18: 191-201.

*Gaudreau, L. (1991). Event-related brain potentials and pupillary responses using a cognitive task in monozygotic twins.  Unpublished doctoral dissertation, City University of New York, New York.

*Gavriysky, V.S. (1991). Human pupillary light reflex and reaction time at different intensity of light stimulation. International Journal of Psychophysiology, 11: 261-268.

Goldwater, B. (1972). Psychological significance of pupillary movements. Psychological Bulletin, 77: 340-355.

*Granholm, E., Asarnow, R.F., Sarkin, A.J., & Dykes, K.L.  (1996). Pupillary responses index cognitive resource limitations. Psychophysiology, 33: 457-461.

*Granholm, E., Chock, D., & Morris, S. Pupillary responses evoked during verbal fluency tasks indicate semantic network dysfunction in schizophrenia. Journal of Clinical and Experimental Neuropsychology, 20: 856-872.

*Granholm, E., Morris, S., Sarkin, A., Asarnow, R., & Jeste, D. (1998). Pupillary responses index overload of working memory resources in schizophrenia. Journal of Abnormal Psychology, 106: 458-467, 1996.

*Grunberger, J., Linzmayer, L., Dietzel, M. & Saletu, B. (1993) The effect of biologically-active light on the noo- [sic] and thymopsyche and on psychophysiological variables in healthy volunteers. International Journal of Psychophysiology, 15: 27-37.

Hakerem, G. (1967). Pupillography. In P. H. Venables & I. Martin, (Eds.), A Manual of Psychophysiological Methods (pp. 335-349). Amsterdam: North-Holland Publishing Co.

Hakerem, G. (1974). Conceptual stimuli, pupillary dilation and evoked cortical potentials: A review of recent advances. In M.-P. Janisse, (Ed.), Pupillary Dynamics and Behavior (pp. 135-158). New York: Plenum Press.

Hakerem G., & Lidsky, A. (1969). Pupillary reactions to sequences of light and variable dark pulses. Annals of the New York Academy of Sciences, 156: 951-958.

Hakerem G., & Lidsky, A. (1975). Characteristics of pupillary reactivity in psychiatric patients and normal controls. In M. L. Kietzman, S. Sutton, & J. Zubin, (Eds.) Experimental Approaches to Psychopathology, (pp. 61-72). New York: Academic Press.

Hakerem, G., & Sutton, S. (1966). Pupillary response at visual threshold. Nature, 212: 485-486.

Hakerem, G., Sutton, S., & Zubin, J. (1964). Pupillary reactions to light in schizophrenic patients and normals. New York Academy of Sciences, 105: 820-831.

*Hensley, W.E. (1990). Pupillary dilation revisited: The constriction of a nonverbal cue. Journal of Social Behavior & Personality, 5: 97-104.

Hess, E.H. (1964). Attitude and pupil size. Scientific American, 212: 46-54.

Hess, E. H. (1972). Pupillometrics: A method of studying mental, emotional, and sensory processes. In N. S. Greenfield, & R. A. Sternbach (Eds.), Handbook of Psychophysiology (pp. 491-531). New York: Holt, Rinehart & Winston.

Hess, E.H. (1975) The Tell-Tale Eye: How Your Eyes Reveal Hidden Thoughts and Emotions. NY: van Nostrand Reinhold.

Hess, E. H., Beaver, P. W., & Shrout, P. E. (1975). Brightness contrast effects in a pupillometric experiment. Perception & Psychophysics, 18: 125-127.

Hess, E.H., & Petrovich, S.B. (1987). Pupillary behavior in communication. In A.W. Siegman & S. Feldstien (Eds.), Nonverbal Behavior and Communication, 2nd Edition. Hillsdale, NJ: pp. 327-349.

Hess, E. H., & Polt, J. M. (1960). Pupil size as related to interest value of visual stimuli. Science, 132: 349-350.

Hess, E. H., & Polt, J. M. (1964). Pupil size in relation to mental activity during simple problem-solving. Science, 143: 1190-1192.

*Hoeks, B., & Ellenbroek, B.A. (1993). A neural basis for a quantitative pupillary model.  Journal of Psychophysiology, 7: 315-324.

*Hoeks, B., & Levelt, W.J.M. (1992).  Pupillary dilation as a measure of attention:  A quantitative system analysis. Behavior Research Methods Instrumentation & Computers, 25: 16-26.

*Hyoenae, J., Tommola, J, & Alaja, A.-M. (1995). Pupil dilation as a measure of processing load in simultaneous interpretation and other language tasks. Quarterly Journal of Experimental Psychology, 48A: 598-512.

*Iriki, A., Tanaka, M., & Iwamura, Y. (1996) Attention-induced neuronal activity in the monkey somatosensory cortex revealed by pupillometrics. Neuroscience Research, 25: 173-181.

Janisse, M.-P., ed. (1974). Pupillary Dynamics and Behavior.  NY: Plenum Press.

Janisse, M.-P. (1977). Pupillometry: The Psychology of the Pupillary Response. Washington, D.C.: Hemisphere Publishing Co.

*Jennings, J.R., van der Molen, M.W. & Steinhauer,S.R. (1998). Preparing the heart, eye, and brain: Foreperiod length effects in a non-aging paradigm. Psychophysiology, 35: 90-98.

*Just, M., & Carpenter, P.A. (1993). The intensity dimension of thought: Pupillometric indices of sentence processing. Canadian Journal of Psychology, 47: 310-339. (also in J.M. Henderson & M. Singer (Eds.), Reading and Language Processing. Mahwah, NJ: Lawrence Erlbaum Ass., pp. 182-211, 1995).

Kahneman, D., & Beatty, J. (1966). Pupil diameter and load on memory. Science, 154: 1583-1585.

Kahneman, D., & Beatty, J. (1967). Pupillary response in a pitch discrimination task. Perception & Psychophysics, 2: 101-105.

Kahneman, D. (1973). Attention and Effort. Englewood Cliffs, N.J.: Prentice-Hall.

*Kim, M., Schwartz, R.L., & Heilman, K.M. (1998). Lateral asymmetries of pupillary responses. Cortex, 34: 753-762.

*Kim, M., Barrett, A.M., & Heilman, K.M. (1999). Pupillographic findings in neglect. Journal of Neurology, Neurosuyrgery and Psychiatry, 67: 82-85.

 

Kohn, M., & Clynes, M. (1969). Color dynamics of the pupil. In M. Clynes, (Ed.), Rein control, or unidirectional rate sensitivity, a fundamental dynamic and organizing function in biology. Annals of the New York Academy of Sciences, 156: 931-950.

*Lester, D., & Kimmel, H.L. (1989). Autonomic nervous system balance and personality. Personality & Individual Differences, 10: 373-374.

Levine, A., & Schilder, P. (1942). The catatonic pupil. The Journal of Nervous and Mental Disease, 96: 1-12.

Levine, S. (1969). Pupillary dilation as a function of stimulus uncertainty. Unpublished master's thesis, Queens College of the City University of New York.

Libby, W.L., Jr., Lacey, B.C., & Lacey, J.I. (1973). Pupillary and cardiac activity during visual attention. Psychophysiology, 10: 270-294.

Lidsky, A., Hakerem, G., & Sutton, S. (1971). Pupillary reactions to single light pulses in psychiatric patients and normals. The Journal of Nervous and Mental Disease, 153, 286-291.

Loewenfeld, I. E. (1958). Mechanisms of reflex dilatation of the pupil. Documenta Ophthalmologica, 12: 185-448.

*Loewenfeld, I. E. (1993). The Pupil: Anatomy, Physiology, and Clinical Applications. Ames: Iowa State University Press.

Lowenstein, O., & Loewenfeld, I. E. (1962). The pupil. In H. Davson, (Ed.), The Eye, Vol 3., (pp. 231-267). New York: Academic Press.

Lowenstein, O., & Westphal, A. (1933). Experimentelle und klinische Studien zur Physiologie der pupillenbewegungen. Berlin: Karger.

* Lubow, R.E., & Fein, O. (1996). Pupillary size in response to a visual guilty knowledge test: New technique for the detection of deception. Journal of Experimental Psychology: Applied, 2: 164-177.

*Matthews, G., Middleton, W., Gilmartin, B., & Bullimore, M.A. (1991). Pupillary diameter and cognitive load. Journal of Psychophysiology, 5: 265-271.

May, P.R.A. (1948). Pupillary abnormalities in schizophrenia during muscular effort. Journal of Mental Science, 94, 89-98.

Metalis, S. A., Rhoades, B. K., Hess, E. H., & Petrovich, S. B. (1980). Pupillometric assessment of reading using materials in normal and reversed orientation. Journal of Applied Psychology, 65: 359-363.

*Millot, J.L., Brand, G., & Schmitt, A. (1996). Affective attitudes of children and adults in relation to the pupil diameter of a cat: Preliminary data. Anthrozooes, 9: 85-87.

*Miyao, M., Ishihara, S. Ishigaki, H., Sugiura, T., Matsura, E., Furuta, M., & Sakata, T. (1993). Psychology of computer use: XXX. Effects of presentation speed on pupil size using negative and positive CRTs. Perceptual & Motor Skills, 77: 979-984.

*Morris, S.K., Granholm, E., Sarkin, A.J., & Jeste, D.V. (1997). Effects of schizophrenia and aging on pupillographic measures of working memory. Schizophrenia Research, 30: 119-128.

*Morrow, L.A., & Steinhauer, S.R. (1995). Alterations in heart rate and pupillary response in persons with organic solvent exposure. Biological Psychiatry, 37: 721-730.

*Mudd, S., Conway, C.G., & Schindler, D.E. (1990). The eye as music critic: Pupil response and verbal preferences. Studia Psychologica, 32: 23-30.

Nunnally, J. C., Knott, P. D., Duchnowski, A., & Parker, R. (1967). Pupillary response as a general measure of activation. Perception & Psychophysics, 2: 149-150.

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