The visuotopic component of the multisensory map in the deep laminae of the cat superior colliculus

A well-defined map of visual space is located in the deep laminae of the cat superior colliculus. The horizontal meridian is oriented rostral-caudal, while the vertical meridian is oriented perpendicular to it in the rostral third of the structure. This map represents the entire contralateral visual field and extends approximately 40 degrees into ipsilateral visual space. Although the deep-laminae visuotopy is similar to that found in the superficial laminae of the same structure, the topographic register among these maps is most secure rostrally but becomes increasingly poorer at more caudal and lateral locations. The combination of 2 features distinguish the deep-layer visual representation from that found in the superficial laminae and in geniculocortical systems: (1) the constituent visual receptive fields are very large (mean diameter, 66.9 degrees), and (2) the majority (greater than 70%) of the neurons composing it receive nonvisual inputs. Because the visual receptive fields of visual-multisensory neurons are significantly larger than those of neighboring neurons that respond only to visual stimuli, far more visual-multisensory neurons are activated by any given visual stimulus. These data, when coupled with those from previous studies, suggest that, from a functional perspective, deep-laminae visual neurons form one component of an integrated multisensory map, and that their topographic organization is essential for the normal dynamics of multisensory integration.

[1]  B E Stein,et al.  Two visual corticotectal systems in cat. , 1984, Journal of neurophysiology.

[2]  B. Stein,et al.  Topographic organization of somatosensory corticotectal influences in cat. , 1984, Journal of neurophysiology.

[3]  J. V. Gisbergen,et al.  Collicular ensemble coding of saccades based on vector summation , 1987, Neuroscience.

[4]  B. Stein,et al.  Properties of superior colliculus neurons in the golden hamster , 1979, The Journal of comparative neurology.

[5]  R. Mooney,et al.  The projection from the superficial to the deep layers of the superior colliculus: an intracellular horseradish peroxidase injection study in the hamster , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  Ann M. Graybiel,et al.  Anatomical organization of retinotectal afferents in the cat: An autodiographic study , 1975, Brain Research.

[7]  E I Knudsen,et al.  Vision guides the adjustment of auditory localization in young barn owls. , 1985, Science.

[8]  A. Antonini,et al.  The contribution of the corpus callosum to receptive fields in the lateral suprasylvian visual areas of the cat , 1982, Behavioural Brain Research.

[9]  J. Apter,et al.  PROJECTION OF THE RETINA ON SUPERIOR COLLICULUS OF CATS , 1945 .

[10]  J. Mcilwain,et al.  Retinal Y-cell activation of deep-layer cells in superior colliculus of the cat. , 1982, Journal of neurophysiology.

[11]  C. Blakemore,et al.  Developmental plasticity in the visual and auditory representations in the mammalian superior colliculus , 1988, Nature.

[12]  Colin Blakemore,et al.  Functional organization in the superior colliculus of the golden hamster , 1976, The Journal of comparative neurology.

[13]  C. Olson,et al.  Ectosylvian visual area of the cat: Location, retinotopic organization, and connections , 1987, The Journal of comparative neurology.

[14]  B E Stein,et al.  Development of the superior colliculus. , 1984, Annual review of neuroscience.

[15]  J T McIlwain,et al.  Visual receptive fields and their images in superior colliculus of the cat. , 1975, Journal of neurophysiology.

[16]  B. Stein,et al.  Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. , 1986, Journal of neurophysiology.

[17]  W. C. Hall,et al.  Superior Colliculus of the Tree Shrew: A Structural and Functional Subdivision into Superficial and Deep Layers , 1972, Science.

[18]  S. Sherman Visual Fields of Cats with Cortical and Tectal Lesions , 1974, Science.

[19]  A K Moschovakis,et al.  Structure-function relationships in the primate superior colliculus. I. Morphological classification of efferent neurons. , 1988, Journal of neurophysiology.

[20]  B E Stein,et al.  Effects of cooling somatosensory cortex on response properties of tactile cells in the superior colliculus. , 1986, Journal of neurophysiology.

[21]  L. Chalupa,et al.  Responses of visual, somatosensory, and auditory neurones in the golden hamster's superior colliculus , 1977, The Journal of physiology.

[22]  B. Gordon,et al.  Receptive fields in deep layers of cat superior colliculus. , 1973, Journal of neurophysiology.

[23]  V. Casagrande,et al.  Ablation study of the superior colliculus in the tree shrew (Tupaia glis) , 1974, The Journal of comparative neurology.

[24]  D L Sparks,et al.  Sensorimotor integration in the primate superior colliculus. II. Coordinates of auditory signals. , 1987, Journal of neurophysiology.

[25]  A R Palmer,et al.  Cells responsive to free‐field auditory stimuli in guinea‐pig superior colliculus: distribution and response properties. , 1983, The Journal of physiology.

[26]  P. D. Spear,et al.  Receptive-field characteristics of single neurons in lateral suprasylvian visual area of the cat. , 1975, Journal of neurophysiology.

[27]  D. Sparks,et al.  Population coding of saccadic eye movements by neurons in the superior colliculus , 1988, Nature.

[28]  J. K. Harting,et al.  Organization of retinocollicular pathways in the cat , 1976, The Journal of comparative neurology.

[29]  W. H. Rohrer,et al.  Organization of the projection from the superficial to the deep layers of the hamster's superior colliculus as demonstrated by the anterograde transport of Phaseolus vulgaris leucoagglutinin , 1989, The Journal of comparative neurology.

[30]  P Sterling,et al.  Influence of visual cortex on receptive fields in the superior colliculus of the cat. , 1969, Journal of neurophysiology.

[31]  D. Hubel,et al.  Visual area of the lateral suprasylvian gyrus (Clare—Bishop area) of the cat , 1969, The Journal of physiology.

[32]  B. Stein,et al.  Spatial factors determine the activity of multisensory neurons in cat superior colliculus , 1986, Brain Research.

[33]  A. Moschovakis,et al.  Observations on the somatodendritic morphology and axonal trajectory of intracellularly HRP‐Labeled efferent neurons located in the deeper layers of the superior colliculus of the cat , 1985, The Journal of comparative neurology.

[34]  B. Stein,et al.  Effects of neonatal cortical lesions upon the cat superior colliculus , 1975, Brain Research.

[35]  Peter H. Hartline The Optic Tectum of Reptiles: Neurophysiological Studies , 1984 .

[36]  B E Stein,et al.  Relationship between visual and tactile representations in cat superior colliculus. , 1976, Journal of neurophysiology.

[37]  R. M. Beckstead,et al.  The lateral suprasylvian corticotectal projection in cats , 1984, The Journal of comparative neurology.

[38]  B E Stein,et al.  Corticotectal and corticothalamic efferent projections of SIV somatosensory cortex in cat. , 1983, Journal of neurophysiology.

[39]  D. Hubel,et al.  Responses to visual stimulation and relationship between visual, auditory, and somatosensory inputs in mouse superior colliculus. , 1975, Journal of neurophysiology.

[40]  J. Sprague,et al.  Corticofugal projections from the visual cortices to the thalamus, pretectum and superior colliculus in the cat , 1974, The Journal of comparative neurology.

[41]  B. Stein,et al.  Determinants of multisensory integration in superior colliculus neurons. I. Temporal factors , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  B. Stein,et al.  A chronic headholder minimizing facial obstructions , 1983, Brain Research Bulletin.

[43]  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.

[44]  C. Gilbert,et al.  The projections of cells in different layers of the cat's visual cortex , 1975, The Journal of comparative neurology.

[45]  G. Schneider,et al.  Topography of visual and somatosensory projections to the superior colliculus of the golden hamster , 1978, Brain Research.

[46]  B E Stein,et al.  Small lateral suprasylvian cortex lesions produce visual neglect and decreased visual activity in the superior colliculus , 1988, The Journal of comparative neurology.

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

[48]  M. Cynader,et al.  Receptive fields in cat superior colliculus after visual cortex lesions. , 1975, Journal of Physiology.

[49]  J. C. Middlebrooks,et al.  A neural code for auditory space in the cat's superior colliculus , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  L. Palmer,et al.  Visual receptive field properties of cells of the superior colliculus after cortical lesions in the cat. , 1971, Experimental neurology.

[51]  J T McIlwain,et al.  Reciprocity of receptive field images and point images in the superior colliculus of the cat , 1981, The Journal of comparative neurology.

[52]  B E Stein,et al.  Unimodal and multimodal response properties of neurons in the cat's superior colliculus. , 1972, Experimental neurology.

[53]  J. Mcilwain,et al.  Interactions of cortical and retinal projections on single neurons of the cat's superior colliculus. , 1971, Journal of neurophysiology.

[54]  M. Dubin,et al.  Development of receptive-field properties of retinal ganglion cells in kittens. , 1977, Journal of neurophysiology.

[55]  E. Murphy,et al.  Alterations in receptive field properties of superior colliculus cells produced by visual cortex ablation in infant and adult cats , 1976, The Journal of comparative neurology.

[56]  H. R. Clemo,et al.  Auditory cortical projection from the anterior ectosylvian sulcus (Field AES) to the superior colliculus in the cat: an anatomical and electrophysiological study. , 1989, The Journal of comparative neurology.