Physiological properties of the output neurons in the deep layers of the superior colliculus of the rabbit

Using antidromic and orthodromic stimulation techniques, we studied physiological properties of the output neurons in the deep layers of the superior colliculus (SC) of 34 Now Zealand rabbits. SC cells antidromically activated from the contralateral predorsal bundle (PDB) could also be activated by stimulation of the contralateral SC and ipsilateral central lateral nucleus of the thalamus (CL). The majority of these output neurons responded predominantly to the stimulation of the optic nerve, and only a small proportion of the output neurons were responsive to the stimulation of somatosensory and auditory (and/or vestibular) nerves. These results suggest that the orienting reflex might be elicited mainly by visual afferents in the rabbit. The output SC neurons were subject to a 70 ms inhibition after antidromic stimulation of the PDB and a 40 ms inhibition after transsynaptic (orthodromic) stimulation of the optic chiasm (OX), indicating that the output neurons in the deep layers of the SC might be subject to at least two inhibitory circuits. These results are discussed in the context of a putative saccadic suppression circuitry model.

[1]  C. Sawyer,et al.  The rabbit diencephalon in stereotaxic coordinates , 1954, The Journal of comparative neurology.

[2]  P. Dean,et al.  Head and body movements produced by electrical stimulation of superior colliculus in rats: Effects of interruption of crossed tectoreticulospinal pathway , 1986, Neuroscience.

[3]  N. Berman,et al.  Laminar organization of superior colliculus in the rabbit: a study of receptive-field properties of single units. , 1981, Journal of neurophysiology.

[4]  W. C. Hall,et al.  Collateral projections of predorsal bundle cells of the superior colliculus in the rat , 1989, The Journal of comparative neurology.

[5]  Hiroshi Kato,et al.  Intracellular studies of rabbit's superior colliculus , 1977, Brain Research.

[6]  A K Moschovakis,et al.  Structure-function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons. , 1988, Journal of neurophysiology.

[7]  P. Dean,et al.  Functional architecture of rodent superior colliculus: relevance of multiple output channels. , 1993, Progress in brain research.

[8]  W. C. Hall,et al.  Anterograde degeneration study of the superior colliculus in Tupaia glis: Evidence for a subdivision between superficial and deep layers , 1973, The Journal of comparative neurology.

[9]  P. Latour.  Visual threshold during eye movements , 1962 .

[10]  M. Behan,et al.  Intrinsic circuitry in the cat superior colliculus: Projections from the superficial layers , 1992, The Journal of comparative neurology.

[11]  B. Stein,et al.  The Merging of the Senses , 1993 .

[12]  B. Gustafsson,et al.  Effect of membrane polarization and synaptic activity on the timing of antidromic invasion , 1980, Brain Research.

[13]  G. W. Beeler,et al.  Visual threshold changes resulting from spontaneous saccadic eye movements. , 1967, Vision research.

[14]  R. Rhoades,et al.  The spinal and commissural projections from the superior colliculus in rat and hamster arise from distinct neuronal populations , 1987, Brain Research.

[15]  J. Rafols,et al.  Intermediate and deep layers of the macaque superior colliculus: A golgi study , 1990, The Journal of comparative neurology.

[16]  S. Lindstro¨m.  Synaptic organization of inhibitory pathways to principal cells in the lateral geniculate nucleus of the cat , 1982, Brain Research.

[17]  M. Jacquin,et al.  The structural and functional characteristics of tectospinal neurons in the golden hamster , 1987, The Journal of comparative neurology.

[18]  G. Ahlsén,et al.  Projection of brain stem neurons to the perigeniculate nucleus and the lateral geniculate nucleus in the cat , 1982, Brain Research.

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

[20]  D. Burr,et al.  Selective suppression of the magnocellular visual pathway during saccadic eye movements , 1994, Nature.

[21]  R. Wurtz,et al.  The Neurobiology of Saccadic Eye Movements , 1989 .

[22]  H Collewijn,et al.  Changes in visual evoked responses during the fast phase of optokinetic nystagmus in the rabbit. , 1969, Vision research.

[23]  M. Schlag-Rey,et al.  The central thalamus. , 1989, Reviews of oculomotor research.

[24]  J. K. Harting,et al.  The Mammalian Superior Colliculus: Studies of Its Morphology and Connections , 1984 .

[25]  M. Wallace,et al.  Converging influences from visual, auditory, and somatosensory cortices onto output neurons of the superior colliculus. , 1993, Journal of neurophysiology.

[26]  H. Vanegas,et al.  Comparative neurology of the optic tectum , 1984 .

[27]  W. C. Hall,et al.  The Anatomical Basis for Sensorimotor Transformations in the Superior Colliculus , 1984 .

[28]  G. Krauthamer,et al.  Somatosensory neurons projecting from the superior colliculus to the intralaminar thalamus in the rat , 1990, Brain Research.

[29]  J. Mcilwain.  Visual input to commissural neurons of the cat's superior colliculus , 1991, Visual Neuroscience.

[30]  M. Conley,et al.  Functional organization of the ventral lateral geniculate complex of the tree shrew (Tupaia belangeri): II. Connections with the cortex, thalamus, and brainstem , 1993, The Journal of comparative neurology.

[31]  B E Stein,et al.  Nociceptive neurons in rat superior colliculus: response properties, topography, and functional implications. , 1989, Journal of neurophysiology.

[32]  A. Aguayo,et al.  Retinal ganglion cell terminals in the hamster superior colliculus: An ultrastructural study , 1991, The Journal of comparative neurology.

[33]  W. D. Neff.  Contributions to sensory physiology , 1965 .