Abstract
OBJECTIVES—Recovery to normal or near normal visual acuity is usual after acute demyelinating optic neuritis, despite the frequent persistence of conduction abnormalities as evidenced by the visual evoked potential (VEP). This raises the possibility that cortical adaptation to a persistently abnormal input contributes to the recovery process. The objective of this study was to investigate the pattern of cerebral response to a simple visual stimulus in recovered patients in comparison to normal subjects. METHODS—Functional magnetic resonance imaging (fMRI) was used to study the brain activation pattern induced by a periodic monocular 8Hz photic stimulus in seven patients who had recovered from a single episode of acute unilateral optic neuritis, and in seven normal controls. VEPs and structural optic nerve MRI were performed on patients. RESULTS—Stimulation of either eye in controls activated only the occipital visual cortex. However, in patients, stimulation of the recovered eye also induced extensive activation in other areas including the insula-claustrum, lateral temporal and posterior parietal cortices, and thalamus; stimulation of the clinically unaffected eye activated visual cortex and right insula-claustrum only. The volume of extraoccipital activation in patients was strongly correlated with VEP latency (r=0.71, p=0.005). CONCLUSIONS—The extraoccipital areas that were activated in patients all have extensive visual connections, and some have been proposed as sites of multimodal sensory integration. The results indicate a functional reorganisation of the cerebral response to simple visual stimuli after optic neuritis that may represent an adaptive response to a persistently abnormal input. Whether this is a necessary part of the recovery process remains to be determined.
Full Text
The Full Text of this article is available as a PDF (274.7 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Berthier M., Starkstein S., Leiguarda R. Behavioral effects of damage to the right insula and surrounding regions. Cortex. 1987 Dec;23(4):673–678. doi: 10.1016/s0010-9452(87)80057-6. [DOI] [PubMed] [Google Scholar]
- Brammer M. J., Bullmore E. T., Simmons A., Williams S. C., Grasby P. M., Howard R. J., Woodruff P. W., Rabe-Hesketh S. Generic brain activation mapping in functional magnetic resonance imaging: a nonparametric approach. Magn Reson Imaging. 1997;15(7):763–770. doi: 10.1016/s0730-725x(97)00135-5. [DOI] [PubMed] [Google Scholar]
- Brusa A., Mortimer C., Jones S. J. Clinical evaluation of VEPs to interleaved checkerboard reversal stimulation of central, hemi- and peripheral fields. Electroencephalogr Clin Neurophysiol. 1995 Nov;96(6):485–494. doi: 10.1016/0013-4694(95)00152-o. [DOI] [PubMed] [Google Scholar]
- Bullmore E. T., Brammer M. J., Rabe-Hesketh S., Curtis V. A., Morris R. G., Williams S. C., Sharma T., McGuire P. K. Methods for diagnosis and treatment of stimulus-correlated motion in generic brain activation studies using fMRI. Hum Brain Mapp. 1999;7(1):38–48. doi: 10.1002/(SICI)1097-0193(1999)7:1<38::AID-HBM4>3.0.CO;2-Q. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bullmore E. T., Rabe-Hesketh S., Morris R. G., Williams S. C., Gregory L., Gray J. A., Brammer M. J. Functional magnetic resonance image analysis of a large-scale neurocognitive network. Neuroimage. 1996 Aug;4(1):16–33. doi: 10.1006/nimg.1996.0026. [DOI] [PubMed] [Google Scholar]
- Bullmore E. T., Suckling J., Overmeyer S., Rabe-Hesketh S., Taylor E., Brammer M. J. Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans Med Imaging. 1999 Jan;18(1):32–42. doi: 10.1109/42.750253. [DOI] [PubMed] [Google Scholar]
- Bullmore E., Brammer M., Williams S. C., Rabe-Hesketh S., Janot N., David A., Mellers J., Howard R., Sham P. Statistical methods of estimation and inference for functional MR image analysis. Magn Reson Med. 1996 Feb;35(2):261–277. doi: 10.1002/mrm.1910350219. [DOI] [PubMed] [Google Scholar]
- Ciaramitaro V. M., Todd W. E., Rosenquist A. C. Disinhibition of the superior colliculus restores orienting to visual stimuli in the hemianopic field of the cat. J Comp Neurol. 1997 Nov 3;387(4):568–587. doi: 10.1002/(sici)1096-9861(19971103)387:4<568::aid-cne7>3.0.co;2-0. [DOI] [PubMed] [Google Scholar]
- Compston D. A., Batchelor J. R., Earl C. J., McDonald W. I. Factors influencing the risk of multiple sclerosis developing in patients with optic neuritis. Brain. 1978 Sep;101(3):495–511. doi: 10.1093/brain/101.3.495. [DOI] [PubMed] [Google Scholar]
- Gareau P. J., Gati J. S., Menon R. S., Lee D., Rice G., Mitchell J. R., Mandelfino P., Karlik S. J. Reduced visual evoked responses in multiple sclerosis patients with optic neuritis: comparison of functional magnetic resonance imaging and visual evoked potentials. Mult Scler. 1999 Jun;5(3):161–164. doi: 10.1177/135245859900500304. [DOI] [PubMed] [Google Scholar]
- Gass A., Barker G. J., MacManus D., Sanders M., Riordan-Eva P., Tofts P. S., Thorpe J., McDonald W. I., Moseley I. F., Miller D. H. High resolution magnetic resonance imaging of the anterior visual pathway in patients with optic neuropathies using fast spin echo and phased array local coils. J Neurol Neurosurg Psychiatry. 1995 May;58(5):562–569. doi: 10.1136/jnnp.58.5.562. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gitelman D. R., Nobre A. C., Parrish T. B., LaBar K. S., Kim Y. H., Meyer J. R., Mesulam M. A large-scale distributed network for covert spatial attention: further anatomical delineation based on stringent behavioural and cognitive controls. Brain. 1999 Jun;122(Pt 6):1093–1106. doi: 10.1093/brain/122.6.1093. [DOI] [PubMed] [Google Scholar]
- Hadjikhani N., Roland P. E. Cross-modal transfer of information between the tactile and the visual representations in the human brain: A positron emission tomographic study. J Neurosci. 1998 Feb 1;18(3):1072–1084. doi: 10.1523/JNEUROSCI.18-03-01072.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Halliday A. M., McDonald W. I., Mushin J. Delayed visual evoked response in optic neuritis. Lancet. 1972 May 6;1(7758):982–985. doi: 10.1016/s0140-6736(72)91155-5. [DOI] [PubMed] [Google Scholar]
- Jones S. J. Visual evoked potentials after optic neuritis. Effect of time interval, age and disease dissemination. J Neurol. 1993 Sep;240(8):489–494. doi: 10.1007/BF00874118. [DOI] [PubMed] [Google Scholar]
- MCDONALD W. I. THE EFFECTS OF EXPERIMENTAL DEMYELINATION ON CONDUCTION IN PERIPHERAL NERVE: A HISTOLOGICAL AND ELECTROPHYSIOLOGICAL STUDY. II. ELECTROPHYSIOLOGICAL OBSERVATIONS. Brain. 1963 Sep;86:501–524. doi: 10.1093/brain/86.3.501. [DOI] [PubMed] [Google Scholar]
- Mesulam M. M. From sensation to cognition. Brain. 1998 Jun;121(Pt 6):1013–1052. doi: 10.1093/brain/121.6.1013. [DOI] [PubMed] [Google Scholar]
- Mufson E. J., Mesulam M. M. Thalamic connections of the insula in the rhesus monkey and comments on the paralimbic connectivity of the medial pulvinar nucleus. J Comp Neurol. 1984 Jul 20;227(1):109–120. doi: 10.1002/cne.902270112. [DOI] [PubMed] [Google Scholar]
- Nieoullon A., Cheramy A., Glowinski J. Release of dopamine evoked by electrical stimulation of the motor and visual areas of the cerebral cortex in both caudate nuclei and in the substantia nigra in the cat. Brain Res. 1978 Apr 21;145(1):69–83. doi: 10.1016/0006-8993(78)90797-7. [DOI] [PubMed] [Google Scholar]
- Olson C. R., Graybiel A. M. Sensory maps in the claustrum of the cat. Nature. 1980 Dec 4;288(5790):479–481. doi: 10.1038/288479a0. [DOI] [PubMed] [Google Scholar]
- Rombouts S. A., Lazeron R. H., Scheltens P., Uitdehaag B. M., Sprenger M., Valk J., Barkhof F. Visual activation patterns in patients with optic neuritis: an fMRI pilot study. Neurology. 1998 Jun;50(6):1896–1899. doi: 10.1212/wnl.50.6.1896. [DOI] [PubMed] [Google Scholar]
- Thomas C. G., Menon R. S. Amplitude response and stimulus presentation frequency response of human primary visual cortex using BOLD EPI at 4 T. Magn Reson Med. 1998 Aug;40(2):203–209. doi: 10.1002/mrm.1910400206. [DOI] [PubMed] [Google Scholar]
- Tsumoto T., Suda K. Effects of stimulation of the dorsocaudal claustrum on activities of striate cortex neurons in the cat. Brain Res. 1982 May 27;240(2):345–349. doi: 10.1016/0006-8993(82)90233-5. [DOI] [PubMed] [Google Scholar]
- Varela F. J., Singer W. Neuronal dynamics in the visual corticothalamic pathway revealed through binocular rivalry. Exp Brain Res. 1987;66(1):10–20. doi: 10.1007/BF00236196. [DOI] [PubMed] [Google Scholar]
- Youl B. D., Turano G., Miller D. H., Towell A. D., MacManus D. G., Moore S. G., Jones S. J., Barrett G., Kendall B. E., Moseley I. F. The pathophysiology of acute optic neuritis. An association of gadolinium leakage with clinical and electrophysiological deficits. Brain. 1991 Dec;114(Pt 6):2437–2450. doi: 10.1093/brain/114.6.2437. [DOI] [PubMed] [Google Scholar]
