1932

Abstract

Patients with homonymous hemianopia sometimes show preservation of the central visual fields, ranging up to 10°. This phenomenon, known as macular sparing, has sparked perpetual controversy. Two main theories have been offered to explain it. The first theory proposes a dual representation of the macula in each hemisphere. After loss of one occipital lobe, the back-up representation in the remaining occipital lobe is postulated to sustain ipsilateral central vision in the blind hemifield. This theory is supported by studies showing that some midline retinal ganglion cells project to the wrong hemisphere, presumably driving neurons in striate cortex that have ipsilateral receptive fields. However, more recent electrophysiological recordings and neuroimaging studies have cast doubt on this theory by showing only a minuscule ipsilateral field representation in early visual cortical areas. The second theory holds that macular sparing arises because the occipital pole, where the macula is represented, remains perfused after occlusion of the posterior cerebral artery because it receives collateral flow from the middle cerebral artery. An objection to this theory is that it cannot account for reports of macular sparing in patients after loss of an entire occipital lobe. On close scrutiny, such reports turn out to be erroneous, arising from inadequate control of fixation during visual field testing. Patients seem able to detect test stimuli on their blind side within the macula or along the vertical meridian because they make surveillance saccades. A purported treatment for hemianopia, called vision restoration therapy, is based on this error. The dual perfusion theory is supported by anatomical studies showing that the middle cerebral artery perfuses the occipital pole in many individuals.In patients with hemianopia from stroke, neuroimaging shows preservation of the occipital pole when macular sparing is present. The frontier dividing the infarcted territory of the posterior cerebral artery and the preserved territory of the middle cerebral artery is variable, but always falls within the representation of the macula, because the macula is so highly magnified. For physicians, macular sparing was an important neurological sign in acute hemianopia because it signified a posterior cerebral artery occlusion. Modern neuroimaging has supplanted the importance of that clinical sign but at the same time confirmed its validity. For patients, macular sparing remains important because it mitigates the impact of hemianopia and preserves the ability to read fluently.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-vision-100119-125406
2021-09-15
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/vision/7/1/annurev-vision-100119-125406.html?itemId=/content/journals/10.1146/annurev-vision-100119-125406&mimeType=html&fmt=ahah

Literature Cited

  1. Adams DL, Piserchia V, Economides JR, Horton JC. 2015. Vascular supply of the cerebral cortex is specialized for cell layers but not columns. Cereb. Cortex 25:3673–81
    [Google Scholar]
  2. Adams DL, Sincich LC, Horton JC. 2007. Complete pattern of ocular dominance columns in human primary visual cortex. J. Neurosci. 27:10391–403
    [Google Scholar]
  3. Andrews TJ, Halpern SD, Purves D. 1997. Correlated size variations in human visual cortex, lateral geniculate nucleus, and optic tract. J. Neurosci. 17:2859–68
    [Google Scholar]
  4. Angelucci A, Bijanzadeh M, Nurminen L, Federer F, Merlin S, Bressloff PC. 2017. Circuits and mechanisms for surround modulation in visual cortex. Annu. Rev. Neurosci. 40:425–51
    [Google Scholar]
  5. Balliet R, Blood KM, Bach-y-Rita P. 1985. Visual field rehabilitation in the cortically blind?. J. Neurol. Neurosurg. Psychiatry 48:1113–24
    [Google Scholar]
  6. Beevor CE. 1909. On the distribution of the different arteries supplying the human brain. Philos. Trans. R. Soc. Lond. B 200:1–55
    [Google Scholar]
  7. Bischoff P, Lang J, Huber A. 1995. Macular sparing as a perimetric artifact. Am. J. Ophthalmol. 119:72–80
    [Google Scholar]
  8. Brewer AA, Press WA, Logothetis NK, Wandell BA. 2002. Visual areas in macaque cortex measured using functional magnetic resonance imaging. J. Neurosci. 22:10416–26
    [Google Scholar]
  9. Briggs F, Usrey WM. 2011. Distinct mechanisms for size tuning in primate visual cortex. J. Neurosci. 31:12644–49
    [Google Scholar]
  10. Brodmann K. 1918. Individuelle Variationen der Sehsphäre und ihr Bedeutung für die Klinik der Hinterhauptschüsse. Allgz. Psychiat 74:564–68
    [Google Scholar]
  11. Brozici M, van der Zwan A, Hillen B. 2003. Anatomy and functionality of leptomeningeal anastomoses: a review. Stroke 34:2750–62
    [Google Scholar]
  12. Cavanaugh MR, Huxlin KR. 2017. Visual discrimination training improves Humphrey perimetry in chronic cortically induced blindness. Neurology 88:1856–64
    [Google Scholar]
  13. Cheng K, Waggoner RA, Tanaka K. 2001. Human ocular dominance columns as revealed by high-field functional magnetic resonance imaging. Neuron 32:359–74
    [Google Scholar]
  14. Cherici C, Kuang X, Poletti M, Rucci M. 2012. Precision of sustained fixation in trained and untrained observers. J. Vis. 12:631
    [Google Scholar]
  15. Clark VP, Courchesne E, Grafe M. 1992. In vivo myeloarchitectonic analysis of human striate and extrastriate cortex using magnetic resonance imaging. Cereb. Cortex 2:417–24
    [Google Scholar]
  16. Cowey A. 1964. Projection of the retina on to striate and prestriate cortex in the squirrel monkey, Saimirisciureus. J. Neurophysiol. 27:366–93
    [Google Scholar]
  17. Coyle JT, Milam DF Jr. 1977. Tangent screen perimetry using twin test objects. Am. J. Ophthalmol. 83:923–24
    [Google Scholar]
  18. Daniel PM, Whitteridge D. 1961. The representation of the visual field on the cerebral cortex in monkeys. J. Physiol. 159:203–21
    [Google Scholar]
  19. DeYoe EA, Carman GJ, Bandettini P, Glickman S, Wieser J et al. 1996. Mapping striate and extrastriate visual areas in human cerebral cortex. PNAS 93:2382–86
    [Google Scholar]
  20. Dougherty RF, Koch VM, Brewer AA, Fischer B, Modersitzki J, Wandell BA. 2003. Visual field representations and locations of visual areas V1/2/3 in human visual cortex. J. Vis. 3:10586–98
    [Google Scholar]
  21. Dow BM, Vautin RG, Bauer R. 1985. The mapping of visual space onto foveal striate cortex in the macaque monkey. J. Neurosci. 5:890–902
    [Google Scholar]
  22. Dubois-Poulsen A, Magis C, de Ajuriaguerra J, Hecaen H. 1952. Les consequences visuelles de la lobectomie occipital chez l'homme. Ann. Ocul. 185:305–47
    [Google Scholar]
  23. Engel SA, Glover GH, Wandell BA. 1997. Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb. Cortex 7:181–92
    [Google Scholar]
  24. Filimonoff I. 1932. Über die Variabilität der Grosshirnrindenstruktur. Regio occipitalis beim erwachsenen Menschen. J. Psychol. Neurol. 44:1–96
    [Google Scholar]
  25. Förster O. 1890. Ueber Rindenblindheit. Arch. Ophthalmol. 36:94–108
    [Google Scholar]
  26. Förster O. 1929. Beiträge zur Pathophysiologie der Sehbahn und der Sehsphäre. J. Psychol. Neurol. 39:463–85
    [Google Scholar]
  27. Förster R. 1867. Über Gesichtsfeldmessungen. Klin. Monatsbl. Augenh 5:293
    [Google Scholar]
  28. Foulsham T, Teszka R, Kingstone A. 2011. Saccade control in natural images is shaped by the information visible at fixation: evidence from asymmetric gaze-contingent windows. Atten. Percept. Psychophysiol. 73:266–83
    [Google Scholar]
  29. Fukuda Y, Sawai H, Watanabe M, Wakakuwa K, Morigiwa K. 1989. Nasotemporal overlap of crossed and uncrossed retinal ganglion cell projections in the Japanese monkey (Macacafuscata). J. Neurosci. 9:2353–73
    [Google Scholar]
  30. Gibaldi A, Benson NC, Banks MS. 2021. Crossed–uncrossed projections from primate retina are adapted to disparities of natural scenes. PNAS 118:e2015651118
    [Google Scholar]
  31. Glickstein M. 1988. The discovery of the visual cortex. Sci. Am. 259:118–27
    [Google Scholar]
  32. Glickstein M, Whitteridge D. 1987. Tatsuji Inouye and the mapping of the visual fields on the human cerebral cortex. Trends Neurosci 10:350–53
    [Google Scholar]
  33. Gonzalez EG, Wong AM, Niechwiej-Szwedo E, Tarita-Nistor L, Steinbach MJ. 2012. Eye position stability in amblyopia and in normal binocular vision. Investig. Ophthalmol. Vis. Sci. 53:5386–94
    [Google Scholar]
  34. Gray LG, Galetta SL, Siegal T, Schatz NJ. 1997. The central visual field in homonymous hemianopia. Evidence for unilateral foveal representation. Arch. Neurol. 54:312–17
    [Google Scholar]
  35. Gross CG, Rocha-Miranda CE, Bender DB. 1972. Visual properties of neurons in inferotemporal cortex of the macaque. J. Neurophysiol. 35:96–111
    [Google Scholar]
  36. Hallum LE, Movshon JA. 2014. Surround suppression supports second-order feature encoding by macaque V1 and V2 neurons. Vis. Res. 104:24–35
    [Google Scholar]
  37. Halstead WC, Walker AE, Bucy PC. 1940. Sparing and nonsparing of “macular” vision associated with occipital lobectomy in man. Arch. Ophthalmol. 24:948–66
    [Google Scholar]
  38. Henry CA, Joshi S, Xing D, Shapley RM, Hawken MJ. 2013. Functional characterization of the extraclassical receptive field in macaque V1: contrast, orientation, and temporal dynamics. J. Neurosci. 33:6230–42
    [Google Scholar]
  39. Henschen SE. 1900. Revue Critique de la Doctrine sur le Centre Cortical de la Vision Paris: G. Steinheil
  40. Holmes G. 1945. The Ferrier Lecture: the organization of the visual cortex in man. Proc. R. Soc. Lond. B 132:348–61
    [Google Scholar]
  41. Holmes G, Lister WT. 1916. Disturbances of vision from cerebral lesions, with special reference to the cortical representation of the macula. Brain 39:34
    [Google Scholar]
  42. Holmes GM. 1918. Disturbances of vision by cerebral lesions. Br. J. Ophthalmol. 2:353
    [Google Scholar]
  43. Horton JC, Adams DL. 2018. Patterns of cortical visual field defects from embolic stroke explained by the anastomotic organization of vascular microlobules. J. Neuroophthalmol. 38:538–50
    [Google Scholar]
  44. Horton JC, Fahle M, Mulder T, Trauzettel-Klosinski S. 2017. Adaptation, perceptual learning, and plasticity of brain functions. Graefes Arch. Clin. Exp. Ophthalmol. 255:435–47
    [Google Scholar]
  45. Horton JC, Hoyt WF. 1991. The representation of the visual field in human striate cortex: a revision of the classic Holmes map. Arch. Ophthalmol. 109:816–24
    [Google Scholar]
  46. Huber A. 1962. Homonymous hemianopia after occipital lobectomy. Am. J. Ophthalmol. 54:623–29
    [Google Scholar]
  47. Inouye T. 1909. Die Sehstörungen bei Schussverletzungen der kortikalen Sehsphäre nach Beobachtungen an Verwundeten der letzten japanischen Kriege Leipzig, Ger: W. Engelmann
  48. Juba A. 1934. Die korticale Doppelvertretung der Makula und die Projektion der Sehrinde auf den äusseren Kniehöcker des Menschen. Klin. Monatsbl. Augenh 93:595
    [Google Scholar]
  49. Kamyar R, Trobe JD. 2009. Bilateral mesial occipital lobe infarction after cardiogenic hypotension induced by electrical shock. J. Neuroophthalmol. 29:107–10
    [Google Scholar]
  50. Kasten E, Wust S, Behrens-Baumann W, Sabel BA. 1998. Computer-based training for the treatment of partial blindness. Nat. Med. 4:1083–87
    [Google Scholar]
  51. Kölliker A. 1899. Neue Beobachtungen zur Anatomie des chiasma opticum. Beiträge zur Onkologie des Auges J von Michel 113–28 Würzburg, Ger: Phys.-Med. Ges.
    [Google Scholar]
  52. Lanyon LJ, Barton JJ. 2013. Visual search and line bisection in hemianopia: computational modelling of cortical compensatory mechanisms and comparison with hemineglect. PLOS ONE 8:e54919
    [Google Scholar]
  53. Leff A. 2004. A historical review of the representation of the visual field in primary visual cortex with special reference to the neural mechanisms underlying macular sparing. Brain Lang 88:268–78
    [Google Scholar]
  54. Leff AP, Scott SK, Crewes H, Hodgson TL, Cowey A et al. 2000. Impaired reading in patients with right hemianopia. Ann. Neurol. 47:171–78
    [Google Scholar]
  55. Leventhal AG, Ault SJ, Vitek DJ. 1988. The nasotemporal division in primate retina: the neural bases of macular sparing and splitting. Science 240:66–67
    [Google Scholar]
  56. Mansouri B, Roznik M, Rizzo JF III, Prasad S 2018. Rehabilitation of visual loss: where we are and where we need to be. J. Neuroophthalmol. 38:223–29
    [Google Scholar]
  57. Marchand F. 1882. Beitrag zur Kenntniss der homonymen bilateralen Hemianopsie und der Faserkreuzung im Chiasma opticum. Arch. Ophthalmol 28:63
    [Google Scholar]
  58. Margolis MT, Newton TH, Hoyt WF. 1971. Cortical branches of the posterior cerebral artery. Anatomic-radiologic correlation. Neuroradiology 2:127–35
    [Google Scholar]
  59. Marinkovic SV, Milisavljevic MM, Lolic-Draganic V, Kovacevic MS. 1987. Distribution of the occipital branches of the posterior cerebral artery. Correlation with occipital lobe infarcts. Stroke 18:728–32
    [Google Scholar]
  60. McAuley DL, Russell RW. 1979. Correlation of CAT scan and visual field defects in vascular lesions of the posterior visual pathways. J. Neurol. Neurosurg. Psychiatry 42:298–311
    [Google Scholar]
  61. McFadzean R, Brosnahan D, Hadley D, Mutlukan E. 1994. Representation of the visual field in the occipital striate cortex. Br. J. Ophthalmol. 78:185–90
    [Google Scholar]
  62. Meienberg O, Zangemeister WH, Rosenberg M, Hoyt WF, Stark L. 1981. Saccadic eye movement strategies in patients with homonymous hemianopia. Ann. Neurol. 9:537–44
    [Google Scholar]
  63. Ogawa K, Ishikawa H, Suzuki Y, Oishi M, Kamei S. 2014. Clinical study of the visual field defects caused by occipital lobe lesions. Cerebrovasc. Dis. 37:102–8
    [Google Scholar]
  64. Otero-Millan J, Macknik SL, Martinez-Conde S. 2014. Fixational eye movements and binocular vision. Front. Integr. Neurosci. 8:52
    [Google Scholar]
  65. Pambakian A, Currie J, Kennard C. 2005. Rehabilitation strategies for patients with homonymous visual field defects. J. Neuroophthalmol. 25:136–42
    [Google Scholar]
  66. Pambakian AL, Kennard C. 1997. Can visual function be restored in patients with homonymous hemianopia?. Br. J. Ophthalmol. 81:324–28
    [Google Scholar]
  67. Pambakian AL, Wooding DS, Patel N, Morland AB, Kennard C, Mannan SK. 2000. Scanning the visual world: a study of patients with homonymous hemianopia. J. Neurol. Neurosurg. Psychiatry 69:751–59
    [Google Scholar]
  68. Papageorgiou E, Hardiess G, Mallot HA, Schiefer U. 2012. Gaze patterns predicting successful collision avoidance in patients with homonymous visual field defects. Vis. Res. 65:25–37
    [Google Scholar]
  69. Penfield W, Evans JP, MacMillan JA. 1935. Visual pathways in man with particular reference to macular representation. Arch. Neurol. Psychiatry 33:816–34
    [Google Scholar]
  70. Pessin MS, Lathi ES, Cohen MB, Kwan ES, Hedges TR III, Caplan LR. 1987. Clinical features and mechanism of occipital infarction. Ann. Neurol. 21:290–99
    [Google Scholar]
  71. Plant GT. 2005. A work out for hemianopia. Br. J. Ophthalmol. 89:2
    [Google Scholar]
  72. Pollock A, Hazelton C, Rowe FJ, Jonuscheit S, Kernohan A et al. 2019. Interventions for visual field defects in people with stroke. Cochrane Database Syst. Rev. 5:CD008388
    [Google Scholar]
  73. Polyak S. 1933. A contribution to the cerebral representation of the retina. J. Comp. Neurol. 57:541–67
    [Google Scholar]
  74. Polyak S. 1957. The Vertebrate Visual System Chicago: Univ. Chicago Press
  75. Ramon y Cajal S. 1911. Histologie du Système Nerveux de L'Homme et Des Vertébrés Paris: A. Maloine
  76. Reinhard J, Schreiber A, Schiefer U, Kasten E, Sabel BA et al. 2005. Does visual restitution training change absolute homonymous visual field defects? A fundus controlled study. Br. J. Ophthalmol. 89:30–35
    [Google Scholar]
  77. Reinhard J, Trauzettel-Klosinski S. 2003. Nasotemporal overlap of retinal ganglion cells in humans: a functional study. Investig. Ophthalmol. Vis. Sci. 44:1568–72
    [Google Scholar]
  78. Reinhard JI, Damm I, Ivanov IV, Trauzettel-Klosinski S. 2014. Eye movements during saccadic and fixation tasks in patients with homonymous hemianopia. J. Neuroophthalmol. 34:354–61
    [Google Scholar]
  79. Rosenholtz R. 2016. Capabilities and limitations of peripheral vision. Annu. Rev. Vis. Sci. 2:437–57
    [Google Scholar]
  80. Sereno MI, Dale AM, Reppas JB, Kwong KK, Belliveau JW et al. 1995. Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268:889–93
    [Google Scholar]
  81. Smirnakis SM. 2016. Probing human visual deficits with functional magnetic resonance imaging. Annu. Rev. Vis. Sci. 2:171–95
    [Google Scholar]
  82. Smith CG, Richardson WF. 1966. The course and distribution of the arteries supplying the visual (striate) cortex. Am. J. Ophthalmol. 61:1391–96
    [Google Scholar]
  83. Snyder JP. 1993. Flattening the Earth: Two Thousand Years of Map Projections Chicago: Univ. Chicago Press
  84. Stensaas SS, Eddington DK, Dobelle WH. 1974. The topography and variability of the primary visual cortex in man. J. Neurosurg. 40:747–55
    [Google Scholar]
  85. Strbian D, Ahmed N, Wahlgren N, Kaste M, Tatlisumak T. 2012. Intravenous thrombolysis in ischemic stroke patients with isolated homonymous hemianopia: analysis of Safe Implementation of Thrombolysis in Stroke-International Stroke Thrombolysis Register (SITS-ISTR). Stroke 43:2695–98
    [Google Scholar]
  86. Sugishita M, Hemmi I, Sakuma I, Beppu H, Shiokawa Y. 1993. The problem of macular sparing after unilateral occipital lesions. J. Neurol. 241:1–9
    [Google Scholar]
  87. Symon L. 1961. Studies of leptomeningeal collateral circulation in Macacusrhesus. J. Physiol. 159:68–86.1
    [Google Scholar]
  88. Taban M, Heller KB, Hsu HY, Sadun AA. 2005. Bifurcating axons account for the increase in axonal population in posterior human optic nerve. Neuro-Ophthalmology 29:109–14
    [Google Scholar]
  89. Talbot SA, Marshall WH. 1941. Physiological studies on neural mechanisms of visual localization and discrimination. Am. J. Ophthalmol. 24:1255–64
    [Google Scholar]
  90. Tanaka R, Miyasaka Y, Yada K, Mukuno K. 1992. Bilateral homonymous hemianopsia due to tentorial herniation, with sparing of central vision: case report. Neurosurgery 31:787–90
    [Google Scholar]
  91. Teuber HL, Battersby NS, Bender MF. 1960. Visual Field Defects After Penetrating Missile Wounds of the Brain Cambridge, MA: Harvard Univ. Press
  92. Tootell RB, Mendola JD, Hadjikhani NK, Liu AK, Dale AM 1998. The representation of the ipsilateral visual field in human cerebral cortex. PNAS 95:818–24
    [Google Scholar]
  93. Tootell RB, Switkes E, Silverman MS, Hamilton SL. 1988. Functional anatomy of macaque striate cortex. II. Retinotopic organization. J. Neurosci. 8:1531–68
    [Google Scholar]
  94. Trampel R, Bazin PL, Pine K, Weiskopf N. 2019. In-vivo magnetic resonance imaging (MRI) of laminae in the human cortex. NeuroImage 197:707–15
    [Google Scholar]
  95. Traquair HM. 1925. The special vulnerability of the macular fibers and “sparing of the macula. .” Br. J. Ophthalmol. 9:53–57
    [Google Scholar]
  96. Trauzettel-Klosinski S, Brendler K. 1998. Eye movements in reading with hemianopic field defects: the significance of clinical parameters. Graefes Arch. Clin. Exp. Ophthalmol. 236:91–102
    [Google Scholar]
  97. Trauzettel-Klosinski S, Reinhard J 1998. The vertical field border in hemianopia and its significance for fixation and reading. Investig. Ophthalmol. Vis. Sci. 39:2177–86
    [Google Scholar]
  98. van der Zwan A, Hillen B, Tulleken CA, Dujovny M, Dragovic L. 1992. Variability of the territories of the major cerebral arteries. J. Neurosurg. 77:927–40
    [Google Scholar]
  99. Van Essen DC, Newsome WT, Maunsell JH. 1984. The visual field representation in striate cortex of the macaque monkey: asymmetries, anisotropies, and individual variability. Vis. Res. 24:429–48
    [Google Scholar]
  100. Wall M, Schiefer U. 2018. Reader response: visual discrimination training improves Humphrey perimetry in chronic cortically induced blindness. Neurology 90:436–37
    [Google Scholar]
  101. Wandell BA, Winawer J. 2011. Imaging retinotopic maps in the human brain. Vis. Res. 51:718–37
    [Google Scholar]
  102. Wilbrand H, Saenger A. 1904. Die Neurologie des Auges, Vol. 3 Wiesbaden, Ger: J. Bergmann
  103. Wilbrand H, Saenger A. 1917. Die homonyme Hemianopsie nebst ihren Beziehungen zu den anderen cerebralen Herderscheinungen, Vol. 7 Wiesbaden, Ger: J. Bergmann
  104. Wong AM, Sharpe JA. 1999. Representation of the visual field in the human occipital cortex: a magnetic resonance imaging and perimetric correlation. Arch. Ophthalmol. 117:208–17
    [Google Scholar]
  105. Wong-Riley MT. 1989. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci 12:94–101
    [Google Scholar]
  106. Zarella MD, Ts'o DY 2017. Contextual modulation revealed by optical imaging exhibits figural asymmetry in macaque V1 and V2. Eye Brain 9:1–12
    [Google Scholar]
  107. Zeal AA, Rhoton AL Jr. 1978. Microsurgical anatomy of the posterior cerebral artery. J. Neurosurg. 48:534–59
    [Google Scholar]
  108. Zhang X, Kedar S, Lynn MJ, Newman NJ, Biousse V. 2006. Homonymous hemianopias: clinical-anatomic correlations in 904 cases. Neurology 66:906–10
    [Google Scholar]
  109. Zihl J, von Cramon D. 1982. Restitution of visual field in patients with damage to the geniculostriate visual pathway. Hum. Neurobiol. 1:5–8
    [Google Scholar]
/content/journals/10.1146/annurev-vision-100119-125406
Loading
/content/journals/10.1146/annurev-vision-100119-125406
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error