Skip to main content
Erschienen in: Graefe's Archive for Clinical and Experimental Ophthalmology 9/2017

30.06.2017 | Neurophthalmology

Chromatic pupillography in hemianopia patients with homonymous visual field defects

verfasst von: Fumiatsu Maeda, Carina Kelbsch, Torsten Straßer, Karolína Skorkovská, Tobias Peters, Barbara Wilhelm, Helmut Wilhelm

Erschienen in: Graefe's Archive for Clinical and Experimental Ophthalmology | Ausgabe 9/2017

Einloggen, um Zugang zu erhalten

Abstract

Purpose

The pupil light reflex is considered to be a simple subcortical reflex. However, many studies have proven that patients with isolated occipital lesions with homonymous hemianopia show pupillary hemihypokinesia. Our hypothesis is that the afferent pupillary system consists of two pathways: one via intrinsically photosensitive retinal ganglion cells (ipRGCs), the other running through the normal RGCs via the visual cortex. The purpose of this study was to test the hypothesis of these two separate pupillomotor pathways.

Methods

12 patients (59.1 ± 18.8 years) with homonymous hemianopia due to post-geniculate lesions of the visual pathway and 20 normal controls (58.6 ± 12.9 years) were examined using chromatic pupillography: stimulus intensity was 28 lx corneal illumination, stimulus duration was 4.0 s, and the stimulus wavelengths were 420 ± 20 nm (blue) and 605 ± 20 nm (red), respectively. The examined parameters were baseline pupil diameter, latency, and relative amplitudes (absolute amplitudes compared to baseline), measured at maximal constriction, at 3 s after stimulus onset, at stimulus offset, and at 3 s and 7 s after stimulus offset.

Results

The relative amplitudes for the red stimulus were significantly smaller for hemianopia patients compared to the normal controls [maximal constriction: 35.6 ± 5.9% (hemianopia) to 42.3 ± 5.7% (normal); p = 0.004; 3 s after stimulus onset: p = 0.004; stimulus offset: p = 0.001]. No significant differences in any parameter were found between the two groups using the blue stimulus.

Conclusions

The results support the hypothesis that the ipRGC pathway is mainly subcortical, whereas a second, non-ipRGC pathway via the occipital cortex exists.
Literatur
1.
Zurück zum Zitat Alexandridis E, Krastel H, Reuther R (1979) Disturbances of the pupil reflex associated with lesions of the upper visual pathway (author's transl). Albrecht Von Graefes Arch Klin Exp Ophthalmol 209:199–208CrossRefPubMed Alexandridis E, Krastel H, Reuther R (1979) Disturbances of the pupil reflex associated with lesions of the upper visual pathway (author's transl). Albrecht Von Graefes Arch Klin Exp Ophthalmol 209:199–208CrossRefPubMed
2.
Zurück zum Zitat Barris RW (1936) A pupillo-constrictor area in the cerebral cortex of the cat and its relationship to the pretectal area. J Comp Neurol 63:353–368CrossRef Barris RW (1936) A pupillo-constrictor area in the cerebral cortex of the cat and its relationship to the pretectal area. J Comp Neurol 63:353–368CrossRef
3.
Zurück zum Zitat Berson DM, Dunn FA, Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070–1073CrossRefPubMed Berson DM, Dunn FA, Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070–1073CrossRefPubMed
4.
Zurück zum Zitat Bridge H, Jindahra P, Barbur J et al (2011) Imaging reveals optic tract degeneration in hemianopia. Invest Ophthalmol Vis Sci 52:382–388CrossRefPubMed Bridge H, Jindahra P, Barbur J et al (2011) Imaging reveals optic tract degeneration in hemianopia. Invest Ophthalmol Vis Sci 52:382–388CrossRefPubMed
5.
Zurück zum Zitat Cibis GW, Campos EC, Aulhorn E (1975) Pupillary hemiakinesia in suprageniculate lesions. Arch Ophthalmol 93:1322–1327CrossRefPubMed Cibis GW, Campos EC, Aulhorn E (1975) Pupillary hemiakinesia in suprageniculate lesions. Arch Ophthalmol 93:1322–1327CrossRefPubMed
6.
Zurück zum Zitat Dacey DM, Liao HW, Peterson BB et al (2005) Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433:749–754CrossRefPubMed Dacey DM, Liao HW, Peterson BB et al (2005) Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433:749–754CrossRefPubMed
7.
Zurück zum Zitat Distler C, Hoffmann KP (1989) The pupillary light reflex in normal and innate microstrabismic cats, II: retinal and cortical input to the nucleus praetectalis olivaris. Vis Neurosci 3:139–153CrossRefPubMed Distler C, Hoffmann KP (1989) The pupillary light reflex in normal and innate microstrabismic cats, II: retinal and cortical input to the nucleus praetectalis olivaris. Vis Neurosci 3:139–153CrossRefPubMed
8.
Zurück zum Zitat Gamlin PD, Mcdougal DH, Pokorny J et al (2007) Human and macaque pupil responses driven by melanopsin-containing retinal ganglion cells. Vis Res 47:946–954CrossRefPubMedPubMedCentral Gamlin PD, Mcdougal DH, Pokorny J et al (2007) Human and macaque pupil responses driven by melanopsin-containing retinal ganglion cells. Vis Res 47:946–954CrossRefPubMedPubMedCentral
9.
Zurück zum Zitat Gooley JJ, Lu J, Chou TC et al (2001) Melanopsin in cells of origin of the retinohypothalamic tract. Nat Neurosci 4:1165CrossRefPubMed Gooley JJ, Lu J, Chou TC et al (2001) Melanopsin in cells of origin of the retinohypothalamic tract. Nat Neurosci 4:1165CrossRefPubMed
10.
Zurück zum Zitat Goto K, Miki A, Yamashita T et al (2015) Sectoral analysis of the retinal nerve fiber layer thinning and its association with visual field loss in homonymous hemianopia caused by post-geniculate lesions using spectral-domain optical coherence tomography. Graefes Arch Clin Exp Ophthalmol Goto K, Miki A, Yamashita T et al (2015) Sectoral analysis of the retinal nerve fiber layer thinning and its association with visual field loss in homonymous hemianopia caused by post-geniculate lesions using spectral-domain optical coherence tomography. Graefes Arch Clin Exp Ophthalmol
11.
Zurück zum Zitat Harms H (1949) Grundlagen, Methodik und Bedeutung der Pupillenperimetrie für die Physiologie und Pathologie des Sehorgans. Albrecht v Graefes Arch Ophthal 149:1–68CrossRef Harms H (1949) Grundlagen, Methodik und Bedeutung der Pupillenperimetrie für die Physiologie und Pathologie des Sehorgans. Albrecht v Graefes Arch Ophthal 149:1–68CrossRef
12.
Zurück zum Zitat Harms H (1951) Hemianopic pupillary rigidity. Klin Monbl Augenheilkd Augenarztl Fortbild 118:133–147PubMed Harms H (1951) Hemianopic pupillary rigidity. Klin Monbl Augenheilkd Augenarztl Fortbild 118:133–147PubMed
13.
Zurück zum Zitat Hattar S, Kumar M, Park A et al (2006) Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol 497:326–349CrossRefPubMedPubMedCentral Hattar S, Kumar M, Park A et al (2006) Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol 497:326–349CrossRefPubMedPubMedCentral
14.
Zurück zum Zitat Hattar S, Liao HW, Takao M et al (2002) Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295:1065–1070CrossRefPubMedPubMedCentral Hattar S, Liao HW, Takao M et al (2002) Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295:1065–1070CrossRefPubMedPubMedCentral
15.
Zurück zum Zitat Hellner KA, Jensen W, Muller-Jensen A (1978) Videoprocessing pupillographic perimetry in hemianopsia (author's transl). Klin Monatsbl Augenheilkd 172:731–735PubMed Hellner KA, Jensen W, Muller-Jensen A (1978) Videoprocessing pupillographic perimetry in hemianopsia (author's transl). Klin Monatsbl Augenheilkd 172:731–735PubMed
16.
Zurück zum Zitat Heywood CA, Nicholas JJ, Lemare C et al (1998) The effect of lesions to cortical areas V4 or AIT on pupillary responses to chromatic and achromatic stimuli in monkeys. Exp Brain Res 122:475–480CrossRefPubMed Heywood CA, Nicholas JJ, Lemare C et al (1998) The effect of lesions to cortical areas V4 or AIT on pupillary responses to chromatic and achromatic stimuli in monkeys. Exp Brain Res 122:475–480CrossRefPubMed
17.
Zurück zum Zitat Inoue T, Kiribuchi T (1985) Cortical and subcortical pathways for pupillary reactions in rabbits. Jpn J Ophthalmol 29:63–70PubMed Inoue T, Kiribuchi T (1985) Cortical and subcortical pathways for pupillary reactions in rabbits. Jpn J Ophthalmol 29:63–70PubMed
18.
Zurück zum Zitat Ishikawa H, Onodera A, Asakawa K et al (2012) Effects of selective-wavelength block filters on pupillary light reflex under red and blue light stimuli. Jpn J Ophthalmol 56:181–186CrossRefPubMed Ishikawa H, Onodera A, Asakawa K et al (2012) Effects of selective-wavelength block filters on pupillary light reflex under red and blue light stimuli. Jpn J Ophthalmol 56:181–186CrossRefPubMed
19.
Zurück zum Zitat Jindahra P, Petrie A, Plant GT (2009) Retrograde trans-synaptic retinal ganglion cell loss identified by optical coherence tomography. Brain 132:628–634CrossRefPubMed Jindahra P, Petrie A, Plant GT (2009) Retrograde trans-synaptic retinal ganglion cell loss identified by optical coherence tomography. Brain 132:628–634CrossRefPubMed
20.
Zurück zum Zitat Jindahra P, Petrie A, Plant GT (2012) Thinning of the retinal nerve fibre layer in homonymous Quadrantanopia: further evidence for retrograde trans-synaptic degeneration in the human visual system. Neuro-Ophthalmology 36:79–84CrossRef Jindahra P, Petrie A, Plant GT (2012) Thinning of the retinal nerve fibre layer in homonymous Quadrantanopia: further evidence for retrograde trans-synaptic degeneration in the human visual system. Neuro-Ophthalmology 36:79–84CrossRef
21.
Zurück zum Zitat Jindahra P, Petrie A, Plant GT (2012) The time course of retrograde trans-synaptic degeneration following occipital lobe damage in humans. Brain 135:534–541CrossRefPubMed Jindahra P, Petrie A, Plant GT (2012) The time course of retrograde trans-synaptic degeneration following occipital lobe damage in humans. Brain 135:534–541CrossRefPubMed
22.
Zurück zum Zitat Kardon R, Anderson SC, Damarjian TG et al (2009) Chromatic pupil responses: preferential activation of the melanopsin-mediated versus outer photoreceptor-mediated pupil light reflex. Ophthalmology 116:1564–1573CrossRefPubMed Kardon R, Anderson SC, Damarjian TG et al (2009) Chromatic pupil responses: preferential activation of the melanopsin-mediated versus outer photoreceptor-mediated pupil light reflex. Ophthalmology 116:1564–1573CrossRefPubMed
24.
Zurück zum Zitat Keenleyside M, Barbur J, Pinney H (1988) Stimulus-specific pupillary responses in normal and hemianopic subjects. Perception 17:347 Keenleyside M, Barbur J, Pinney H (1988) Stimulus-specific pupillary responses in normal and hemianopic subjects. Perception 17:347
25.
Zurück zum Zitat Loewenfeld IE (1993) The pupil: anatomy, physiology, and clinical applications. Iowa State University Press and Wayne State University Press Loewenfeld IE (1993) The pupil: anatomy, physiology, and clinical applications. Iowa State University Press and Wayne State University Press
26.
Zurück zum Zitat Lucas RJ, Hattar S, Takao M et al (2003) Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science 299:245–247CrossRefPubMed Lucas RJ, Hattar S, Takao M et al (2003) Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science 299:245–247CrossRefPubMed
27.
Zurück zum Zitat Mcdougal DH, Gamlin PD (2010) The influence of intrinsically-photosensitive retinal ganglion cells on the spectral sensitivity and response dynamics of the human pupillary light reflex. Vis Res 50:72–87CrossRefPubMedPubMedCentral Mcdougal DH, Gamlin PD (2010) The influence of intrinsically-photosensitive retinal ganglion cells on the spectral sensitivity and response dynamics of the human pupillary light reflex. Vis Res 50:72–87CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat Panda S, Sato TK, Castrucci AM et al (2002) Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 298:2213–2216CrossRefPubMed Panda S, Sato TK, Castrucci AM et al (2002) Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 298:2213–2216CrossRefPubMed
30.
Zurück zum Zitat Papageorgiou E, Ticini LF, Hardiess G et al (2008) The pupillary light reflex pathway: cytoarchitectonic probabilistic maps in hemianopic patients. Neurology 70:956–963CrossRefPubMed Papageorgiou E, Ticini LF, Hardiess G et al (2008) The pupillary light reflex pathway: cytoarchitectonic probabilistic maps in hemianopic patients. Neurology 70:956–963CrossRefPubMed
31.
Zurück zum Zitat Provencio I, Rollag MD, Castrucci AM (2002) Photoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from night. Nature 415:493CrossRefPubMed Provencio I, Rollag MD, Castrucci AM (2002) Photoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from night. Nature 415:493CrossRefPubMed
32.
Zurück zum Zitat Schmid R, Luedtke H, Wilhelm BJ et al (2005) Pupil campimetry in patients with visual field loss. Eur J Neurol 12:602–608CrossRefPubMed Schmid R, Luedtke H, Wilhelm BJ et al (2005) Pupil campimetry in patients with visual field loss. Eur J Neurol 12:602–608CrossRefPubMed
33.
Zurück zum Zitat Skorkovská K, Maeda F, Kelbsch C et al (2014) Pupillary response to chromatic stimuli. Cesk Slov Neurol N 77(110):334–338 Skorkovská K, Maeda F, Kelbsch C et al (2014) Pupillary response to chromatic stimuli. Cesk Slov Neurol N 77(110):334–338
34.
Zurück zum Zitat Skorkovska K, Wilhelm H, Ludtke H et al (2009) How sensitive is pupil campimetry in hemifield loss? Graefes Arch Clin Exp Ophthalmol 247:947–953CrossRefPubMed Skorkovska K, Wilhelm H, Ludtke H et al (2009) How sensitive is pupil campimetry in hemifield loss? Graefes Arch Clin Exp Ophthalmol 247:947–953CrossRefPubMed
35.
Zurück zum Zitat Steele GE, Weller RE (1993) Subcortical connections of subdivisions of inferior temporal cortex in squirrel monkeys. Vis Neurosci 10:563–583CrossRefPubMed Steele GE, Weller RE (1993) Subcortical connections of subdivisions of inferior temporal cortex in squirrel monkeys. Vis Neurosci 10:563–583CrossRefPubMed
36.
Zurück zum Zitat Tanito M, Ohira A (2013) Hemianopic inner retinal thinning after stroke. Acta Ophthalmol 91:e237–e238CrossRefPubMed Tanito M, Ohira A (2013) Hemianopic inner retinal thinning after stroke. Acta Ophthalmol 91:e237–e238CrossRefPubMed
37.
Zurück zum Zitat Walker CB (1913) Topical diagnostic value of the hemiopic pupillary reaction and the wilbrand hemianoptic prism phenomenon: with a new method of performing the latter. J Am Med Assoc 61:1152–1156CrossRef Walker CB (1913) Topical diagnostic value of the hemiopic pupillary reaction and the wilbrand hemianoptic prism phenomenon: with a new method of performing the latter. J Am Med Assoc 61:1152–1156CrossRef
38.
Zurück zum Zitat Wernicke C (1883) Über hemianopische Pupillenreaktion. Fortschr Med 1:9–53 Wernicke C (1883) Über hemianopische Pupillenreaktion. Fortschr Med 1:9–53
39.
Zurück zum Zitat Wilhelm BJ, Wilhelm H, Moro S et al (2002) Pupil response components: studies in patients with Parinaud's syndrome. Brain 125:2296–2307CrossRefPubMed Wilhelm BJ, Wilhelm H, Moro S et al (2002) Pupil response components: studies in patients with Parinaud's syndrome. Brain 125:2296–2307CrossRefPubMed
40.
Zurück zum Zitat Wilhelm H, Kardon RH (1997) The pupillary light reflex pathway. Neuro-Ophthalmology 17:59–62CrossRef Wilhelm H, Kardon RH (1997) The pupillary light reflex pathway. Neuro-Ophthalmology 17:59–62CrossRef
41.
Zurück zum Zitat Wilhelm H, Wilhelm B, Petersen D et al (1996) Relative afferent pupillary defects in patients with geniculate and retrogeniculate lesions. Neuro-Ophthalmology 16:219–224CrossRef Wilhelm H, Wilhelm B, Petersen D et al (1996) Relative afferent pupillary defects in patients with geniculate and retrogeniculate lesions. Neuro-Ophthalmology 16:219–224CrossRef
42.
Zurück zum Zitat Yamashita T, Miki A, Iguchi Y et al (2012) Reduced retinal ganglion cell complex thickness in patients with posterior cerebral artery infarction detected using spectral-domain optical coherence tomography. Jpn J Ophthalmol 56:502–510CrossRefPubMed Yamashita T, Miki A, Iguchi Y et al (2012) Reduced retinal ganglion cell complex thickness in patients with posterior cerebral artery infarction detected using spectral-domain optical coherence tomography. Jpn J Ophthalmol 56:502–510CrossRefPubMed
43.
Zurück zum Zitat Yoshitomi T, Matsui T, Tanakadate A et al (1999) Comparison of threshold visual perimetry and objective pupil perimetry in clinical patients. J Neuroophthalmol 19:89–99CrossRefPubMed Yoshitomi T, Matsui T, Tanakadate A et al (1999) Comparison of threshold visual perimetry and objective pupil perimetry in clinical patients. J Neuroophthalmol 19:89–99CrossRefPubMed
Metadaten
Titel
Chromatic pupillography in hemianopia patients with homonymous visual field defects
verfasst von
Fumiatsu Maeda
Carina Kelbsch
Torsten Straßer
Karolína Skorkovská
Tobias Peters
Barbara Wilhelm
Helmut Wilhelm
Publikationsdatum
30.06.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
Graefe's Archive for Clinical and Experimental Ophthalmology / Ausgabe 9/2017
Print ISSN: 0721-832X
Elektronische ISSN: 1435-702X
DOI
https://doi.org/10.1007/s00417-017-3721-y

Weitere Artikel der Ausgabe 9/2017

Graefe's Archive for Clinical and Experimental Ophthalmology 9/2017 Zur Ausgabe

Neu im Fachgebiet Augenheilkunde

Update Augenheilkunde

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.