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Effects of fixational saccades on response timing in macaque lateral geniculate nucleus

Published online by Cambridge University Press:  08 October 2010

ALAN B. SAUL*
Affiliation:
Department of Ophthalmology, Medical College of Georgia, Augusta, Georgia
*
*Address correspondence and reprint requests to: Alan B. Saul, Department of Ophthalmology, Medical College of Georgia, Augusta, GA 30912. E-mail: asaul@mcg.edu

Abstract

Even during active fixation, small eye movements persist that might be expected to interfere with vision. Numerous brain mechanisms probably contribute to discounting this jitter. Changes in the timing of responses in the visual thalamus associated with fixational saccades are considered in this study. Activity of single neurons in alert monkey lateral geniculate nucleus (LGN) was recorded during fixation while pseudorandom visual noise stimuli were presented. The position of the stimulus on the display monitor was adjusted based on eye position measurements to control for changes in retinal locations due to eye movements. A method for extracting nonstationary first-order response mechanisms was applied, so that changes around the times of saccades could be observed. Saccade-related changes were seen in both amplitude and timing of geniculate responses. Amplitudes were greatly reduced around saccades. Timing was retarded slightly during a window of about 200 ms around saccades. That is, responses became more sustained. These effects were found in both parvocellular and magnocellular neurons. Timing changes in LGN might play a role in maintaining cortical responses to visual stimuli in the presence of eye movements, compensating for the spatial shifts caused by saccades via these shifts in timing.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 2010

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References

Anstis, S. & Casco, C. (2006). Induced movement: The flying bluebottle illusion. Journal of Vision 6, 10871092.Google Scholar
Bair, W. & O’Keefe, L.P. (1998). The influence of fixational eye movements on the response of neurons in area MT of the macaque. Visual Neuroscience 15, 779786.Google Scholar
Binda, P., Cicchini, G.M., Burr, D.C. & Morrone, M.C. (2009). Spatiotemporal distortions of visual perception at the time of saccades. The Journal of Neuroscience 29, 1314713157.CrossRefGoogle ScholarPubMed
Crowder, N., Price, N., Mustari, M. & Ibbotson, M. (2009). Direction and contrast tuning of macaque MSTd neurons during saccades. Journal of Neurophysiology 101, 31003107.CrossRefGoogle ScholarPubMed
Desbordes, G. & Rucci, M. (2007). A model of the dynamics of retinal activity during natural visual fixation. Visual Neuroscience 24, 217230.CrossRefGoogle Scholar
Dong, D.W. (2002). Dynamic temporal decorrelation: A theory of saccadic effects on the LGN responses. Investigative Ophthalmology & Visual Science 43, 3929.Google Scholar
Duhamel, J.R., Colby, C.L. & Goldberg, M.E. (1992). The updating of the representation of visual space in parietal cortex by intended eye movements. Science 255, 9092.CrossRefGoogle ScholarPubMed
Greschner, M., Bongard, M., Rujan, P. & Ammermüller, J. (2002). Retinal ganglion cell synchronization by fixational eye movements improves feature estimation. Nature Neuroscience 5, 341347.CrossRefGoogle ScholarPubMed
Gur, M. & Snodderly, D.M. (1987). Studying striate cortex neurons in behaving monkeys: Benefits of image stabilization. Vision Research 27, 20812087.Google Scholar
Gur, M. & Snodderly, D.M. (1997). Visual receptive fields of neurons in primary visual cortex (V1) move in space with the eye movements of fixation. Vision Research 37, 257265.Google Scholar
Ibbotson, M.R., Crowder, N.A., Cloherty, S.L., Price, N.S.C. & Mustari, M.J. (2008). Saccadic modulation of neural responses: Possible roles in saccadic suppression, enhancement, and time compression. The Journal of Neuroscience 28, 1095210960.CrossRefGoogle ScholarPubMed
Ibbotson, M.R., Price, N.S.C., Crowder, N.A., Ono, S. & Mustari, M.J. (2007). Enhanced motion sensitivity follows saccadic suppression in the superior temporal sulcus of the macaque cortex. Cerebral Cortex 17, 11291138.Google Scholar
Kagan, I., Gur, M. & Snodderly, D.M. (2008). Saccades and drifts differentially modulate neuronal activity in V1: Effects of retinal image motion, position, and extraretinal influences. Journal of Vision 8, 125.Google Scholar
Lee, D. & Malpeli, J.G. (1998). Effects of saccades on the activity of neurons in the cat lateral geniculate nucleus. Journal of Neurophysiology 79, 922936.Google Scholar
Leopold, D.A. & Logothetis, N.K. (1998). Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex. Experimental Brain Research 123, 341345.Google Scholar
MacEvoy, S.P., Hanks, T.D. & Paradiso, M.A. (2008). Macaque V1 activity during natural vision: Effects of natural scenes and saccades. Journal of Neurophysiology 99, 460472.Google Scholar
Martinez-Conde, S., Macknik, S.L. & Hubel, D.H. (2002). The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex. Proceedings of the National Academy of Sciences of the United States of America 99, 1392013925.Google Scholar
Martinez-Conde, S., Macknik, S.L. & Hubel, D.H. (2004). The role of fixational eye movements in visual perception. Nature Reviews Neuroscience 5, 229240.Google Scholar
Melcher, D. & Colby, C.L. (2008). Trans-saccadic perception. Trends in Cognitive Science 12, 466473.Google Scholar
Melcher, D. & Morrone, M.C. (2003). Spatiotopic temporal integration of visual motion across saccadic eye movements. Nature Neuroscience 6, 877881.Google Scholar
Morrone, M.C., Ross, J. & Burr, D. (2005). Saccadic eye movements cause compression of time as well as space. Nature Neuroscience 8, 950954.Google Scholar
Murakami, I. (2003). Illusory jitter in a static stimulus surrounded by a synchronously flickering pattern. Vision Research 43, 957969.CrossRefGoogle Scholar
Murakami, I. (2004). Correlations between fixation stability and visual motion sensitivity. Vision Research 44, 751761.CrossRefGoogle ScholarPubMed
Nakamura, K. & Colby, C.L. (2002). Updating of the visual representation in monkey striate and extrastriate cortex during saccades. Proceedings of the National Academy of Sciences of the United States of America 99, 40264031.Google Scholar
Price, N.S.C., Ibbotson, M.R., Ono, S. & Mustari, M.J. (2005). Rapid processing of retinal slip during saccades in macaque area MT. Journal of Neurophysiology 94, 235246.CrossRefGoogle ScholarPubMed
Ramcharan, E.J., Gnadt, J.W. & Sherman, S.M. (2001). The effects of saccadic eye movements on the activity of geniculate relay neurons in the monkey. Visual Neuroscience 18, 253258.Google Scholar
Reppas, J.B., Usrey, W.M. & Reid, R.C. (2002). Saccadic eye movements modulate visual responses in the lateral geniculate nucleus. Neuron 35, 961974.Google Scholar
Rucci, M., Iovin, R., Poletti, M. & Santini, F. (2007). Miniature eye movements enhance fine spatial detail. Nature 447, 851854.Google Scholar
Saul, A.B. (2008 a). Lagged cells in alert monkey lateral geniculate nucleus. Visual Neuroscience 25, 647659.CrossRefGoogle ScholarPubMed
Saul, A.B. (2008 b). Temporal receptive field estimation using wavelets. Journal of Neuroscience Methods 168, 450464.Google Scholar
Saul, A.B. & Humphrey, A.L. (1990). Spatial and temporal response properties of lagged and nonlagged cells in cat lateral geniculate nucleus. Journal of Neurophysiology 64, 206224.Google Scholar
Snodderly, D.M. & Gur, M. (1995). Organization of striate cortex (V1) of alert, trained monkeys (Macaca fascicularis): Ongoing activity, stimulus selectivity, and widths of receptive field activating regions. Journal of Neurophysiology 74, 21002125.Google Scholar
Sylvester, R., Haynes, J.-D. & Rees, G. (2005). Saccades differentially modulate human LGN and V1 responses in the presence and absence of visual stimulation. Current Biology 15, 3741.CrossRefGoogle ScholarPubMed
Sylvester, R. & Rees, G. (2006). Extraretinal saccadic signals in human LGN and early retinotopic cortex. Neuroimage 30, 214219.Google Scholar
Tang, Y., Saul, A., Gur, M., Goei, S., Wong, E., Ersoy, B. & Snodderly, D.M. (2007). Eye position compensation improves estimates of response magnitude and receptive field geometry in alert monkeys. Journal of Neurophysiology 97, 34393448.Google Scholar
Terao, M., Watanabe, J., Yagi, A. & Nishida, S. (2008). Reduction of stimulus visibility compresses apparent time intervals. Nature Neuroscience 11, 541542.CrossRefGoogle ScholarPubMed
Umeno, M.M. & Goldberg, M.E. (1997). Spatial processing in the monkey frontal eye field. I. Predictive visual responses. Journal of Neurophysiology 78, 13731383.Google Scholar
Walker, M.F., Fitzgibbon, E.J. & Goldberg, M.E. (1995). Neurons in the monkey superior colliculus predict the visual result of impending saccadic eye movements. Journal of Neurophysiology 73, 19882003.Google Scholar
Wurtz, R.H. (2008). Neuronal mechanisms of visual stability. Vision Research 48, 20702089.Google Scholar
Wyder, M.T., Massoglia, D.P. & Stanford, T.R. (2003). Quantitative assessment of the timing and tuning of visual-related, saccade-related, and delay period activity in primate central thalamus. Journal of Neurophysiology 90, 20292052.Google Scholar