Abstract
A saccadic eye movement causes a variety of transient perceptual sequelae that might be the results of corollary discharge. Here we describe the neural circuits for saccadic corollary discharge that modulates activity throughout the pigeon visual system. Saccades in pigeons caused inhibition that was mediated by corollary discharge followed by enhancement of firing activity in the telencephalic hyperpallium, visual thalamus and pretectal nucleus lentiformis mesencephali (nLM) with opposite responses in the accessory optic nucleus (nBOR). Inactivation of thalamic neurons eliminated saccadic responses in telencephalic neurons, and inactivation of both the nLM and the nBOR abolished saccadic responses in thalamic neurons. Saccade-related omnipause neurons in the brainstem raphe complex inhibited the nBOR and excited the nLM, whereas inactivation of raphe neurons eliminated saccadic responses in both optokinetic and thalamic neurons. It seems that saccadic responses in telencephalic neurons are generated by corollary discharge signals from brainstem neurons that are transmitted through optokinetic and thalamic neurons. These signals might have important roles in visual perception.
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References
Tolias, A.S. et al. Eye movements modulate visual receptive fields of V4 neurons. Neuron 29, 757–767 (2001).
Kusunoki, M. & Goldberg, M.E. The time course of perisaccadic receptive field shifts in the lateral intraparietal area of the monkey. J. Neurophysiol. 89, 1519–1527 (2003).
Sommer, M.A. & Wurtz, R.H. Influence of the thalamus on spatial visual processing in frontal cortex. Nature 444, 374–377 (2006).
Yarrow, K., Haggard, P., Heal, R., Brown, P. & Rothwell, J.C. Illusory perceptions of space and time preserve cross-saccadic perceptual continuity. Nature 414, 302–305 (2001).
Morrone, M.C., Ross, J. & Burr, D. Saccadic eye movements cause compression of time as well as space. Nat. Neurosci. 8, 950–954 (2005).
Lee, D. & Malpeli, J.G. Effects of saccades on the activity of neurons in the cat lateral geniculate nucleus. J. Neurophysiol. 79, 922–936 (1998).
Reppas, J.B., Usrey, W.M. & Reid, R.C. Saccadic eye movements modulate visual responses in the lateral geniculate nucleus. Neuron 35, 961–974 (2002).
Royal, D.W., Sary, G., Schall, J.D. & Casagrande, V.A. Correlates of motor planning and postsaccadic fixation in the macaque monkey lateral geniculate nucleus. Exp. Brain Res. 168, 62–75 (2006).
Burr, D.C., Morrone, M.C. & Ross, J. Selective suppression of the magnocellular visual pathway during saccadic eye movements. Nature 371, 511–513 (1994).
Ross, J., Burr, D.C. & Morrone, M.C. Suppression of the magnocellular pathways during saccades. Behav. Brain Res. 80, 1–8 (1996).
Thiele, A., Henning, P., Kubischik, M. & Hoffmann, K.P. Neural mechanisms of saccadic suppression. Science 295, 2460–2462 (2002).
Wurtz, R.H. & Sommer, M.A. Identifying corollary discharges for movement in the primate brain. Prog. Brain Res. 144, 47–60 (2004).
Wylie, D.R., Glover, R.G. & Lau, K.L. Projections from the accessory optic system and pretectum to the dorsolateral thalamus in the pigeon (Columbia livia): a study using both anterograde and retrograde tracers. J. Comp. Neurol. 391, 456–469 (1998).
Cao, P., Yang, Y., Yang, Y. & Wang, S.R. Differential modulation of thalamic neurons by optokinetic nuclei in the pigeon. Brain Res. 1069, 159–165 (2006).
McKenna, O.C. & Wallman, J. Accessory optic system and pretectum of birds: comparisons with those of other vertebrates. Brain Behav. Evol. 26, 91–116 (1985).
Shimizu, T. & Bowers, A.N. Visual circuits of the avian telencephalon: evolutionary implications. Behav. Brain Res. 98, 183–191 (1999).
Gioanni, H., Rey, J., Villalobos, J., Richard, D. & Dalbera, A. Optokinetic nystagmus in the pigeon (Columba livia). II. Role of the pretectal nucleus of the accessory optic system (AOS). Exp. Brain Res. 50, 237–247 (1983).
Clement, G. & Magnin, M. Effects of accessory optic system lesions on vestibule-ocular and optokinetic reflexes in the cat. Exp. Brain Res. 55, 49–59 (1984).
Schiff, D., Cohen, B., Buttner-Ennever, J. & Matsuo, V. Effects of lesions of the nucleus of the optic tract on optokinetic nystagmus and after-nystagmus in the monkey. Exp. Brain Res. 79, 225–239 (1990).
Toledo, C.A., Hamassaki-Britto, D.E. & Britto, L.R. Serotonergic afferents of the pigeon accessory optic nucleus. Brain Res. 705, 341–344 (1995).
Reiner, A. & Karten, H.J. Laminar distribution of the cells of origin of the descending tectofugal pathway in the pigeon (Columba livia). J. Comp. Neurol. 204, 165–187 (1982).
Luksch, H. Cytoarchitecture of the avian optic tectum: neuronal substrate for cellular computation. Rev. Neurosci. 14, 85–106 (2003).
Everling, S., Pare, M., Dorris, M.C. & Munoz, D.P. Comparison of the discharge characteristics of brain stem omnipause neurons and superior colliculus fixation neurons in monkey: implications for control of fixation and saccade behavior. J. Neurophysiol. 79, 511–528 (1998).
Brecht, M., Singer, W. & Engel, A.K. Amplitude and direction of saccadic eye movements depend on the synchronicity of collicular population activity. J. Neurophysiol. 92, 424–432 (2004).
Angeles Luque, M., Perez-Perez, M.P., Herrero, L. & Torres, B. Involvement of the optic tectum and mesencephalic reticular formation in the generation of saccadic eye movements in goldfish. Brain Res. Brain Res. Rev. 49, 388–397 (2005).
Sparks, D.L. The brainstem control of saccadic eye movements. Nat. Rev. Neurosci. 3, 952–964 (2002).
Horn, A.K. The reticular formation. Prog. Brain Res. 151, 127–155 (2005).
Pettigrew, J.D., Wallman, J. & Wildsoet, C.F. Saccadic oscillations facilitate ocular perfusion from the avian pecten. Nature 343, 362–363 (1990).
Wohlschläger, A., Jäger, R. & Delius, J.D. Head and eye movements in unrestrained pigeons (Columba livia). J. Comp. Psychol. 107, 313–317 (1993).
Niu, Y.Q., Xiao, Q., Liu, R.F., Wu, L.Q. & Wang, S.R. Response characteristics of the pigeon's pretectal neurons to illusory contours and motion. J. Physiol. (Lond.) 577, 805–813 (2006).
Keller, E.L. Participation of medial pontine reticular formation in eye movement generation in monkey. J. Neurophysiol. 37, 316–332 (1974).
Bagnoli, P. & Burkhalter, A. Organization of the afferent projections to the wulst in the pigeon. J. Comp. Neurol. 214, 103–113 (1983).
Güntürkün, O. & Karten, H.J. An immunocytochemical analysis of the lateral geniculate complex in the pigeon (Columba livia). J. Comp. Neurol. 314, 721–749 (1991).
Koshiba, M., Yohda, M. & Nakamura, S. Topological relation of chick thalamofugal visual projections with hyperpallium revealed by three color tracers. Neurosci. Res. 52, 235–242 (2005).
Brecha, N. & Karten, H.J. Accessory optic projections upon oculomotor nuclei and vestibulocerebellum. Science 203, 913–916 (1979).
Buttner-Ennever, J.A., Cohen, B., Horn, A.K. & Reisine, H. Pretectal projections to the oculomotor complex of the monkey and their role in eye movements. J. Comp. Neurol. 366, 348–359 (1996).
Lisberger, S.G. & Fuchs, A.F. Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth-pursuit eye movements and passive head rotation. J. Neurophysiol. 41, 733–763 (1978).
Lisberger, S.G. Postsaccadic enhancement of initiation of smooth pursuit eye movements in monkeys. J. Neurophysiol. 79, 1918–1930 (1998).
Ibbotson, M.R., Price, N.S., Crowder, N.A., Ono, S. & Mustari, M.J. Enhanced motion sensitivity follows saccadic suppression in the superior temporal sulcus of the macaque cortex. Cereb. Cortex 17, 1129–1138 (2007).
Schmidt, M., Lehnert, G., Baker, R.G. & Hoffmann, K.P. Dendritic morphology of projection neurons in the cat pretectum. J. Comp. Neurol. 369, 520–532 (1996).
Mustari, M.J., Fuchs, A.F. & Pong, M. Response properties of pretectal omnidirectional pause neurons in the behaving primate. J. Neurophysiol. 77, 116–125 (1997).
Fischer, W.H., Schmidt, M. & Hoffmann, K.P. Saccade-induced activity of dorsal lateral geniculate nucleus X- and Y-cells during pharmacological inactivation of the cat pretectum. Vis. Neurosci. 15, 197–210 (1998).
Cao, P., Gu, Y. & Wang, S.R. Visual neurons in the pigeon brain encode the acceleration of stimulus motion. J. Neurosci. 24, 7690–7698 (2004).
Wang, S.R. & Matsumoto, N. Postsynaptic potentials and morphology of tectal cells responding to electrical stimulation of the bullfrog nucleus isthmi. Vis. Neurosci. 5, 479–488 (1990).
Karten, H.J. & Hodos, W. A Stereotaxic Atlas of the Brain of the Pigeon (Columba livia) (The Johns Hopkins Press, Baltimore, Maryland, 1967).
Acknowledgements
We thank S.G. Lisberger of University of California San Francisco for help in editing the manuscript. This work was supported by the National Natural Science Foundation of China (90208008) and by the Chinese Academy of Sciences (KSCX1-YW-R-32 and Brain-Mind Project).
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Yan Yang conducted the experiments throughout, P.C. conducted the first half of the experiments, Yang Yang conducted the second half of the experiments and S.-R.W. supervised the project and wrote the manuscript. All co-authors conducted the data analyses.
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Yang, Y., Cao, P., Yang, Y. et al. Corollary discharge circuits for saccadic modulation of the pigeon visual system. Nat Neurosci 11, 595–602 (2008). https://doi.org/10.1038/nn.2107
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DOI: https://doi.org/10.1038/nn.2107