The pupillary light reflex pathway

Objective: The anatomy of the human pupillary light reflex (PLR) pathway is a matter of debate. The aim of this study was twofold: namely, to investigate the association of a relative afferent pupillary defect (RAPD) in acquired suprageniculate lesions with the location and extent of the cerebral lesions. Further, we suggest a new strategy of lesion analysis by combining established techniques with the stereotaxic probabilistic cytoarchitectonic atlas developed by the Jülich group. Methods: Twenty-three patients with homonymous visual field defects participated in this study. The RAPD was quantified clinically by two independent examiners with graded neutral density filters (swinging flashlight test). Using MRI in each individual, cerebral regions commonly affected in patients with a RAPD but spared in patients without a RAPD were determined and subsequently assessed by using cytoarchitectonic probabilistic maps. Results: A RAPD was present in 10/23 patients. Comparison of patients showing a RAPD vs those not showing a RAPD revealed that a region including the course of the optic radiation at its early beginning in the temporal white matter is commonly associated with a RAPD. Conclusions: It was demonstrated that the pupillary light reflex (PLR) depends on the input of suprageniculate neurons, thus supporting the involvement of a cortical pathway also. The site of integration of cortical signals in relation to the PLR into the pupillomotor pathway may be located suprageniculately in the vicinity of the lateral geniculate nucleus. Moreover, the suggested combination of established lesion analysis techniques with the probabilistic cytoarchitectonic atlas turned out to be a very helpful amelioration of stroke data analyses.

[1]  R. Kardon,et al.  Automated pupil perimetry. Pupil field mapping in patients and normal subjects. , 1991, Ophthalmology.

[2]  W Lewin,et al.  Cortical blindness and the functions of the non-geniculate fibres of the optic tracts. , 1969, Journal of neurology, neurosurgery, and psychiatry.

[3]  N. Miller,et al.  A relative afferent pupillary defect without any visual sensory deficit. , 1998, Archives of ophthalmology.

[4]  K. Amunts,et al.  Advances in cytoarchitectonic mapping of the human cerebral cortex. , 2001, Neuroimaging clinics of North America.

[5]  B. Wilhelm,et al.  Relative afferent pupillary defects in patients with geniculate and retrogeniculate lesions , 1996 .

[6]  T. Hohki,et al.  Optic tract syndrome with relative afferent pupillary defect. , 1991, Japanese Journal of Ophthalmology.

[7]  J. Sprague,et al.  Interaction of Cortex and Superior Colliculus in Mediation of Visually Guided Behavior in the Cat , 1966, Science.

[8]  B. Wilhelm,et al.  Absence of relative afferent pupillary defect and pupillary hemiakinesia in a child with homonymous hemianopia due to ((retro-)geniculate) porencephaly , 1998, The British journal of ophthalmology.

[9]  Y. Honda,et al.  Superior oblique paresis with contralateral relative afferent pupillary defect , 2000, Graefe's Archive for Clinical and Experimental Ophthalmology.

[10]  Prof. Dr. med. habil. Heinrich Harms Grundlagen, Methodik und Bedeutung der Pupillenperimetrie für die Physiologie und Pathologie des Sehorgans , 2004, Albrecht von Graefes Archiv für Ophthalmologie.

[11]  Helmut Wilhelm,et al.  Neuro-ophthalmology of pupillary function – practical guidelines , 1998, Journal of Neurology.

[12]  A. Müller-Jensen,et al.  Videopupillographic and VER investigations in patients with congenital and acquired lesions of the optic radiation. , 1979, Ophthalmologica. Journal international d'ophtalmologie. International journal of ophthalmology. Zeitschrift fur Augenheilkunde.

[13]  H. S. Thompson,et al.  Relative afferent pupillary defect in optic tract hemianopias. , 1978, American journal of ophthalmology.

[14]  D. Eliott,et al.  Fourth nerve paresis and ipsilateral relative afferent pupillary defect without visual sensory disturbance. A sign of contralateral dorsal midbrain disease. , 1991, Journal of clinical neuro-ophthalmology.

[15]  A. Schleicher,et al.  Mapping of Histologically Identified Long Fiber Tracts in Human Cerebral Hemispheres to the MRI Volume of a Reference Brain: Position and Spatial Variability of the Optic Radiation , 1999, NeuroImage.

[16]  N. Miller,et al.  Transsynaptic degeneration. , 1981, Archives of ophthalmology.

[17]  Katrin Amunts,et al.  White matter fiber tracts of the human brain: Three-dimensional mapping at microscopic resolution, topography and intersubject variability , 2006, NeuroImage.

[18]  A. Schleicher,et al.  21 – Quantitative Analysis of Cyto- and Receptor Architecture of the Human Brain , 2002 .

[19]  J. Szentágothai Die innere Gliederung des Oculomotoriuskernes , 1942, Archiv für Psychiatrie und Nervenkrankheiten.

[20]  H. Karnath,et al.  Using human brain lesions to infer function: a relic from a past era in the fMRI age? , 2004, Nature Reviews Neuroscience.

[21]  Alan C. Evans,et al.  Anatomical mapping of functional activation in stereotactic coordinate space , 1992, NeuroImage.

[22]  Helmut Wilhelm,et al.  The Prevalence of Relative Afferent Pupillary Defects in Normal Subjects , 2007, Journal of neuro-ophthalmology : the official journal of the North American Neuro-Ophthalmology Society.

[23]  J. VanBuren TRANS-SYNAPTIC RETROGRADE DEGENERATION IN THE VISUAL SYSTEM OF PRIMATES. , 1963, Journal of neurology, neurosurgery, and psychiatry.

[24]  W. Hoyt,et al.  Occipital lobe dysplasia. Magnetic resonance findings in two cases of isolated congenital hemianopia. , 1985, Archives of ophthalmology.

[25]  R. Kardon,et al.  Pupil perimetry. , 1992, Current opinion in ophthalmology.

[26]  Randy H. Kardon,et al.  The pupillary light reflex pathway , 1997 .

[27]  J. Corbett,et al.  Optic tract syndrome. A review of 21 patients. , 1978, Archives of ophthalmology.

[28]  W. Lagrèze,et al.  Relative afferent pupillary defect with normal vision and vertical strabismus—implications for pupillary pathway anatomy , 2007, Graefe's Archive for Clinical and Experimental Ophthalmology.

[29]  J. Diamond,et al.  Sclerotomy complications following pars plana vitrectomy , 2000, The British journal of ophthalmology.

[30]  H. Teuber,et al.  Visual field defects after missile injuries to the geniculo-striate pathway in man , 1973, Experimental Brain Research.

[31]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[32]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[33]  E. Frohman,et al.  Isolated relative afferent pupillary defect secondary to contralateral midbrain compression. , 2004, Archives of neurology.

[34]  J. Odel,et al.  Relative afferent pupillary defect with normal visual function. , 1990, A M A Archives of Ophthalmology.

[35]  J. Re,et al.  Relative afferent pupillary defect in a lesion of the pretectal afferent pupillary pathway. , 1987 .

[36]  Chris Rorden,et al.  Spatial Normalization of Brain Images with Focal Lesions Using Cost Function Masking , 2001, NeuroImage.

[37]  E. Aulhorn,et al.  Pupillary hemiakinesia in suprageniculate lesions. , 1975, A M A Archives of Ophthalmology.

[38]  C. Ellis Afferent pupillary defect in pineal region tumour. , 1984, Journal of neurology, neurosurgery, and psychiatry.

[39]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[40]  J. M. Buren Trans-synaptic retrograde degeneration in the visual system of primates , 1963, Journal of neurology, neurosurgery, and psychiatry.

[41]  Helmut Wilhelm,et al.  Pupil response components: studies in patients with Parinaud's syndrome. , 2002, Brain : a journal of neurology.

[42]  N. Miller,et al.  Optic tract syndrome. Neuro-ophthalmologic considerations. , 1983, Archives of ophthalmology.