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Pupil Research in Clinical Practice

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Pupil Research in Clinical Practice Masaryk University Brno Faculty of Medicine Department of Optometry and Orthoptics PUPIL RESEARCH IN CLINICAL PRACTICE Habilitation thesis (Collection of Articles) MUDr. Karolína Skorkovská, Ph.D. Brno 2017 Acknowledgment I would like to thank my research co-authors and colleagues, it has been an honour and a privilege working with you over the past years. I am particularly grateful to professors Barbara Wilhelm and Helmut Wilhelm, heads of the pupil laboratory in Tübingen, for their kind leadership and friendship that was crucial for my professional life. I want to thank doc. Svatopluk Synek, CSc. for his support of my fellowship activities in Tübingen and prof. Eva Vlková, CSc. for her permission to apply for habilitation degree in ophthalmology. Most of all I would like to thank my partner, Martin Jansa, and the whole family for their love, patience and support. Abstract Examination of pupils in patients with disorders of the eye, the visual pathway or the central nervous system provides interesting information about the anatomy and pathophysiology of the pupil light reflex. Classically, the pupil light reflex pathway is considered to be a simple reflex arc consisting of the retinal ganglion cells, intercalated neurons in the midbrain, the oculomotor nerve and short ciliary nerves. However, with the discovery of intrinsically photosensitive retinal ganglion cells (ipRGCs), we have learned that the pupillomotor information delivered to the midbrain may originate not only in the outer retinal layer (activation of rods and cones) but also in the inner retinal layer (activation of ipRGCs), and pupillographic measurements in patients with various disorders of the visual pathway support the existence of two pupillomotor channels that drive the pupil light reaction – the subcortical (more primitive, luminance channel associated with the ipRGCs) and the suprageniculate (responds to shifts in structured stimuli, is driven by the rods and cones and receives input from the visual cortex and extrastriate areas). The pupil provides a valuable subject of research to experts in different fields. In ophthalmology, the examination of the pupil light reaction offers a unique objective method of testing the visual pathway function. This habilitation thesis is presented as a collection of published articles with a commentary that introduces into the topic and describes the current state of knowledge. Contents 1 Introduction ........................................................................................................................................... 1 2 Anatomy of the pupil light reflex .......................................................................................................... 2 3 Examination of pupils ............................................................................................................................ 3 Relative afferent pupillary defect and swinging flashlight test ..................................................... 3 3.1.2 Swinging flashlight test in glaucoma ..................................................................................... 4 Pupil perimetry (campimetry) ....................................................................................................... 6 3.2.1 Pupil perimetry in patients with retinitis pigmentosa and functional visual field loss ......... 9 3.2.2 Pupil perimetry in glaucoma ............................................................................................... 14 3.2.3 Pupillomotor receptive fields .............................................................................................. 17 Multifocal pupillography ............................................................................................................. 21 Pupillographic sleepiness test ..................................................................................................... 23 Pharmacological testing in pupillary disorders ........................................................................... 26 4 Pupil light reflex in new light ............................................................................................................... 30 RAPD in optic tract lesions .......................................................................................................... 31 RAPD without visual field loss ..................................................................................................... 32 RAPD in suprageniculate lesions with homonymous visual field defect ..................................... 33 Pupillary hemihypokinesia .......................................................................................................... 34 5 Intrinsically photosensitive retinal ganglion cells................................................................................ 40 Chromatic pupillography ............................................................................................................. 43 5.1.1 Chromatic pupillography in patients with homonymous hemianopia ................................ 47 5.1.2 Chromatic pupillography in glaucoma ................................................................................. 49 6 Conclusion ........................................................................................................................................... 51 7 References ........................................................................................................................................... 52 8 Collection of articles ............................................................................................................................ 63 1 Introduction Examination of pupils is an integral part of a medical examination. It offers an objective evaluation of the functioning of the central nervous system including the visual pathway and as such is of interest particularly to neurologists and ophthalmologists. Further, the pupils are an efferent structure of the sympathetic and parasympathetic nervous systems and as such can be subject to various pharmacological tests of the autonomic nervous system. When we are sleepy, the so-called “pupillary oscillations” on the pupillary edges can be observed and used to measure the level of sleepiness. This method has found use in occupational medicine, sleep medicine and psychology. Therefore, the pupil provides an interesting subject of research to experts in different fields. In ophthalmology, the examination of the pupil light reaction offers a unique objective method of testing the visual pathway function. The pupil light reflex can be tested manually or with automated procedures. Researchers worldwide have developed many different devices to test different aspects of the pupil light reaction under specific conditions and in various diseases. Some of these solutions have been successfully adapted into practice and are produced commercially. Some are available only as prototypes and used mostly for research purposes. Classically, the pupil light reflex pathway is considered a simple reflex arc consisting of the retinal ganglion cells, intercalated neurons in the midbrain, the oculomotor nerve and short ciliary nerves. However, pupil experts have always been aware of some contradictory clinical findings that were subject to debate and could not fully be explained by the widespread belief of the functioning of the pupil light reflex and as a result, the pupil light reflex is no longer considered a pure subcortical reflex arc. Moreover, the pupillary research has received new impetus since the discovery of the melanopsin containing retinal ganglion cells (intrinsically photosensitive retinal ganglion cells, ipRGCs) in 2002. Further development of this knowledge has brought new insights into the understanding of the pupillary behaviour. As part of the research group in Tübingen, Germany I could be part of different projects dealing both with clinical applications and the pathophysiology of the pupil light reflex. The presented habilitation thesis summarizes my work in the field of pupil research. 1 2 Anatomy of the pupil light reflex The neural pathway of the pupillary light reflex as first described by Wernicke [1] in the 1880s consists of four neurons (Fig. 1). Afferent fibers of the retinal ganglion cells travel in the optic nerve and undergo hemidecussation at the chiasm before entering the optic tract. In the posterior third of the optic tract, the pupillomotor fibers separate from the sensory fibers, branch medial via the brachium of the superior colliculus to the lateral geniculate nucleus and synapse in the ipsilateral pretectal nucleus in the dorsal midbrain. Intercalated neurons from each pretectal nucleus then project to both Edinger-Westphal nuclei and parasympathetic fibers from the Edinger Westphal nuclei innervate the iris pupillary sphincter muscle. According to this model, the suprageniculate visual pathway should have no influence on the pupillary light reflex. However, studies in patients with lesions of the retrogeniculate pathway have shown that the pupillary pathway is more complex than previously assumed and the retrogeniculate visual pathway and the visual cortex are also involved in the pupillary light reaction. Fig. 1: The human pupillary pathway as first described by Wernicke consists of four neurons (excluding photoreceptors and bipolar cells in the retina): retinal ganglion cells (1), intercalated neurons in the midbrain (2), oculomotor nerve (3) and short ciliary nerves (4). The simplicity of this model can be no
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