The Superior Colliculus Projection Upon the Macaque Inferior Olive

Abstract Saccade accommodation is a productive model for exploring the role of the cerebellum in behavioral plasticity. In this model, the target is moved during the saccade, gradually inducing a change in the saccade vector as the animal adapts. The climbing fiber pathway from the inferior olive provides a visual error signal generated by the superior colliculus that is believed to be crucial for cerebellar adaptation. However, the primate tecto-olivary pathway has only been explored using large injections of the central portion of the superior colliculus. To provide a more detailed picture, we have made injections of anterograde tracers into various regions of the macaque superior colliculus. As shown previously, large central injections primarily label a dense terminal field within the C subdivision at caudal end of the contralateral medial inferior olive. Several, previously unobserved, sites of sparse terminal labeling were noted: bilaterally in the dorsal cap of Kooy and ipsilaterally in C subdivision of the medial inferior olive. Small, physiologically directed, injections into the rostral, small saccade portion of the superior colliculus produced terminal fields in the same regions of the medial inferior olive, but with decreased density. Small injections of the caudal superior colliculus, where large amplitude gaze changes are encoded, again labeled a terminal field located in the same areas. The lack of a topographic pattern within the main tecto-olivary projection suggests that either the precise vector of the visual error is not transmitted to the vermis, or that encoding of this error is via non-topographic means.

[1]  P. May,et al.  The Substantia Nigra Pars Reticulata Modulates Error-Based Saccadic Learning in Monkeys , 2021, eNeuro.

[2]  Yoshiko Kojima,et al.  How cerebellar motor learning keeps saccades accurate. , 2019, Journal of neurophysiology.

[3]  Yoshiko Kojima,et al.  Elimination of the error signal in the superior colliculus impairs saccade motor learning , 2018, Proceedings of the National Academy of Sciences.

[4]  Yoshiko Kojima,et al.  Change in sensitivity to visual error in superior colliculus during saccade adaptation , 2017, Scientific Reports.

[5]  Yoshiko Kojima,et al.  Cerebellar fastigial nucleus influence on ipsilateral abducens activity during saccades. , 2014, Journal of neurophysiology.

[6]  Albert F. Fuchs,et al.  Effect of inactivation and disinhibition of the oculomotor vermis on saccade adaptation , 2011, Brain Research.

[7]  Albert F. Fuchs,et al.  Effects of GABA agonist and antagonist injections into the oculomotor vermis on horizontal saccades , 2010, Brain Research.

[8]  Y Shinoda,et al.  Topographic organization of excitatory and inhibitory commissural connections in the superior colliculi and their functional roles in saccade generation. , 2010, Journal of neurophysiology.

[9]  Yoshiko Kojima,et al.  Changes in Simple Spike Activity of Some Purkinje Cells in the Oculomotor Vermis during Saccade Adaptation Are Appropriate to Participate in Motor Learning , 2010, The Journal of Neuroscience.

[10]  Yoshiko Kojima,et al.  Subthreshold Activation of the Superior Colliculus Drives Saccade Motor Learning , 2009, The Journal of Neuroscience.

[11]  Yuki Kaku,et al.  Learning Signals from the Superior Colliculus for Adaptation of Saccadic Eye Movements in the Monkey , 2009, The Journal of Neuroscience.

[12]  Ziad M Hafed,et al.  Goal Representations Dominate Superior Colliculus Activity during Extrafoveal Tracking , 2008, The Journal of Neuroscience.

[13]  Y. Shinoda,et al.  Commissural mirror-symmetric excitation and reciprocal inhibition between the two superior colliculi and their roles in vertical and horizontal eye movements. , 2007, Journal of neurophysiology.

[14]  Albert F Fuchs,et al.  Activity changes in monkey superior colliculus during saccade adaptation. , 2007, Journal of neurophysiology.

[15]  Robijanto Soetedjo,et al.  Complex Spike Activity of Purkinje Cells in the Oculomotor Vermis during Behavioral Adaptation of Monkey Saccades , 2006, The Journal of Neuroscience.

[16]  Robijanto Soetedjo,et al.  Distinct short-term and long-term adaptation to reduce saccade size in monkey. , 2006, Journal of neurophysiology.

[17]  Scott E. Bevans,et al.  Effect of visual error size on saccade adaptation in monkey. , 2003, Journal of neurophysiology.

[18]  Adonis Moschovakis,et al.  Density gradients of trans‐synaptically labeled collicular neurons after injections of rabies virus in the lateral rectus muscle of the rhesus monkey , 2002, The Journal of comparative neurology.

[19]  A. Fuchs,et al.  Evidence against a moving hill in the superior colliculus during saccadic eye movements in the monkey. , 2002, Journal of neurophysiology.

[20]  M. Goldberg,et al.  Effect of short-term saccadic adaptation on saccades evoked by electrical stimulation in the primate superior colliculus. , 2002, Journal of neurophysiology.

[21]  A. Fuchs,et al.  Evidence that the superior colliculus participates in the feedback control of saccadic eye movements. , 2002, Journal of neurophysiology.

[22]  Christopher T. Noto,et al.  Characteristics of simian adaptation fields produced by behavioral changes in saccade size and direction. , 1999, Journal of neurophysiology.

[23]  T. Kitama,et al.  An Anatomical Substrate for the Spatiotemporal Transformation , 1998, The Journal of Neuroscience.

[24]  A. Fuchs,et al.  Saccadic gain modification: visual error drives motor adaptation. , 1998, Journal of neurophysiology.

[25]  P. May,et al.  Comparison of the distribution and somatodendritic morphology of tectotectal neurons in the cat and monkey , 1998, Visual Neuroscience.

[26]  D. Munoz,et al.  Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. , 1998, Journal of neurophysiology.

[27]  A. Opstal,et al.  Monkey Superior Colliculus Activity During Short-Term Saccadic Adaptation , 1997, Brain Research Bulletin.

[28]  H. Künzle Connections of the superior colliculus with the tegmentum and the cerebellum in the hedgehog tenrec , 1997, Neuroscience Research.

[29]  A. Fuchs,et al.  Characteristics of saccadic gain adaptation in rhesus macaques. , 1997, Journal of neurophysiology.

[30]  B. Cohen,et al.  Efferent pathways of the nucleus of the optic tract in monkey and their role in eye movements , 1996, The Journal of comparative neurology.

[31]  J. V. Van Gisbergen,et al.  Short-term adaptation of electrically induced saccades in monkey superior colliculus. , 1996, Journal of neurophysiology.

[32]  R. Wurtz,et al.  Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. , 1995, Journal of neurophysiology.

[33]  A. Fuchs,et al.  Anatomical connections of the primate pretectal nucleus of the optic tract , 1994, The Journal of comparative neurology.

[34]  T. Akaike,et al.  The tectorecipient zone in the inferior olivary nucleus in the rat , 1992, The Journal of comparative neurology.

[35]  A. Fuchs,et al.  Visual Signals in the Nucleus of the Optic Tract and Their Brain Stem Destinations a , 1992, Annals of the New York Academy of Sciences.

[36]  P. May,et al.  The laminar distribution of macaque tectobulbar and tectospinal neurons , 1992, Visual Neuroscience.

[37]  R. Matsuzaki,et al.  Topographical organization of climbing fiber pathway from the superior colliculus to cerebellar vermal lobules VI–VII in the cat , 1991, Neuroscience.

[38]  S. Kyuhou,et al.  Topographical organization of the tecto-olivo-cerebellar projection in the cat , 1991, Neuroscience.

[39]  M. Behan,et al.  Sources of subcortical GABAergic projections to the superior colliculus in the cat , 1990, The Journal of comparative neurology.

[40]  K. Hoffmann,et al.  Quantitative analysis of visual receptive fields of neurons in nucleus of the optic tract and dorsal terminal nucleus of the accessory optic tract in macaque monkey. , 1989, Journal of neurophysiology.

[41]  W. C. Hall,et al.  Subcortical connections of the superior colliculus in the mustache bat, Pteronotus parnellii , 1987, The Journal of comparative neurology.

[42]  T Fujikado,et al.  Topography of the oculomotor area of the cerebellar vermis in macaques as determined by microstimulation. , 1987, Journal of neurophysiology.

[43]  M. Behan,et al.  An EM‐autoradiographic and EM‐HRP study of the commissural projection of the superior colliculus in the cat , 1985, The Journal of comparative neurology.

[44]  D. T. Hess,et al.  The tecto-olivo-cerebellar pathway in the rat. , 1982, Brain research.

[45]  J. Courville,et al.  Sources of descending afferents to the inferior olive from the upper brain stem in the cat as revealed by the retrograde transport of horseradish peroxidase , 1981, The Journal of comparative neurology.

[46]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[47]  L. Optican,et al.  Cerebellar-dependent adaptive control of primate saccadic system. , 1980, Journal of neurophysiology.

[48]  David L. Sparks,et al.  Movement fields of saccade-related burst neurons in the monkey superior colliculus , 1980, Brain Research.

[49]  J. T. Weber,et al.  The projection of the superior colliculus upon the inferior olivary complex of the cat: an autoradiographic and horseradish peroxidase study , 1978, Brain Research.

[50]  J. Graham An autoradiographic study of the efferent connections of the superior colliculus in the cat , 1977, The Journal of comparative neurology.

[51]  J. K. Harting Descending pathways from the superior colliculus: An autoradiographic analysis in the rhesus monkey (Macaca mulatta) , 1977, The Journal of comparative neurology.

[52]  David L. Sparks,et al.  Response properties of eye movement-related neurons in the monkey superior colliculus , 1975, Brain Research.

[53]  D. Robinson,et al.  Eye movements evoked by cerebellar stimulation in the alert monkey. , 1973, Journal of neurophysiology.

[54]  D. Robinson Eye movements evoked by collicular stimulation in the alert monkey. , 1972, Vision research.

[55]  R. Wurtz,et al.  Activity of superior colliculus in behaving monkey. 3. Cells discharging before eye movements. , 1972, Journal of neurophysiology.

[56]  Y. Kojima A neuronal process for adaptive control of primate saccadic system. , 2019, Progress in brain research.

[57]  Mayu Takahashi,et al.  Morphological and electrophysiological characteristics of the commissural system in the superior colliculi for control of eye movements. , 2019, Progress in brain research.

[58]  Kaoru Yoshida,et al.  Premotor inhibitory neurons carry signals related to saccade adaptation in the monkey. , 2008, Journal of neurophysiology.

[59]  A. Fuchs,et al.  Complex spike activity signals the direction and size of dysmetric saccade errors. , 2008, Progress in brain research.

[60]  P. May The mammalian superior colliculus: laminar structure and connections. , 2006, Progress in brain research.

[61]  N. Barmack,et al.  Inferior olive and oculomotor system. , 2006, Progress in brain research.