Superior colliculus connections with visual thalamus in gray squirrels (Sciurus carolinensis): Evidence for four subdivisions within the pulvinar complex

As diurnal rodents with a well‐developed visual system, squirrels provide a useful comparison of visual system organization with other highly visual mammals such as tree shrews and primates. Here, we describe the projection pattern of gray squirrel superior colliculus (SC) with the large and well‐differentiated pulvinar complex. Our anatomical results support the conclusion that the pulvinar complex of squirrels consists of four distinct nuclei. The caudal (C) nucleus, distinct in cytochrome oxidase (CO), acetylcholinesterase (AChE), and vesicular glutamate transporter‐2 (VGluT2) preparations, received widespread projections from the ipsilateral SC, although a crude retinotopic organization was suggested. The caudal nucleus also received weaker projections from the contralateral SC. The caudal nucleus also projects back to the ipsilateral SC. Lateral (RLl) and medial (RLm) parts of the previously defined rostral lateral pulvinar (RL) were architectonically distinct, and each nucleus received its own retinotopic pattern of focused ipsilateral SC projections. The SC did not project to the rostral medial (RM) nucleus of the pulvinar. SC injections also revealed ipsilateral connections with the dorsal and ventral lateral geniculate nuclei, nuclei of the pretectum, and nucleus of the brachium of the inferior colliculus and bilateral connections with the parabigeminal nuclei. Comparisons with other rodents suggest that a variously named caudal nucleus, which relays visual inputs from the SC to temporal visual cortex, is common to all rodents and possibly most mammals. RM and RL divisions of the pulvinar complex also appear to have homologues in other rodents. J. Comp. Neurol. 519:1071–1094, 2011. © 2010 Wiley‐Liss, Inc.

[1]  G. Groos,et al.  Cortico-recipient and tecto-recipient visual zones in the rat's lateral posterior (pulvinar) nucleus: An anatomical study , 1981, Neuroscience Letters.

[2]  Stephen D Van Hooser,et al.  The squirrel as a rodent model of the human visual system , 2006, Visual Neuroscience.

[3]  H. Rodman,et al.  Pattern of retinal projections in the California ground squirrel (Spermophilus beecheyi): Anterograde tracing study using cholera toxin , 2003, The Journal of comparative neurology.

[4]  W. C. Hall,et al.  The normal organization of the lateral posterior nucleus of the golden hamster , 1980, The Journal of comparative neurology.

[5]  J. Kaas,et al.  The visual pulvinar in tree shrews I. Multiple subdivisions revealed through acetylcholinesterase and Cat‐301 chemoarchitecture , 2003, The Journal of comparative neurology.

[6]  Diamond It.  Organization of the visual cortex: comparative anatomical and behavioral studies. , 1976 .

[7]  J. K. Harting,et al.  Ascending pathways from the monkey superior colliculus: An autoradiographic analysis , 1980, The Journal of comparative neurology.

[8]  Ann M. Graybiel,et al.  Parallel thalamic zones in the LP-pulvinar complex of the cat identified by their afferent and efferent connections , 1978, Brain Research.

[9]  J M Allman,et al.  Representation of the visual field in the superior colliculus of the grey squirrel (Sciurus carolinensis) and the tree shrew (Tupaia glis). , 1971, Brain research.

[10]  John Q. Trojanowski,et al.  Peroxidase labeled subcortical afferents to pulvinar in rhesus monkey , 1975, Brain Research.

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

[12]  F. Ebner,et al.  Connections of he visual cortex in the hedgehog (Paraechinus hypomelas). II. Corticocortical projections , 1978 .

[13]  A. Graybiel.  A satellite system of the superior colliculus: the parabigeminal nucleus and its projections to the superficial collicular layers , 1978, Brain Research.

[14]  J. Kaas,et al.  Connections of area 2 of somatosensory cortex with the anterior pulvinar and subdivisions of the ventroposterior complex in macaque monkeys , 1985, The Journal of comparative neurology.

[15]  L. P. Morin,et al.  Immunocytochemical characterization of the suprachiasmatic nucleus and the intergeniculate leaflet in the diurnal ground squirrel, Spermophilus lateralis , 1991, Brain Research.

[16]  J. Kaas.  The Evolution of the Dorsal Thalamus in Mammals , 2007 .

[17]  J. T. Weber,et al.  The efferent projections of the pretectal complex: an autoradiographic and horseradish peroxidase analysis , 1980, Brain Research.

[18]  D. Fitzpatrick,et al.  New view of the organization of the pulvinar nucleus in Tupaia as revealed by tectopulvinar and pulvinar‐cortical projections , 1988, The Journal of comparative neurology.

[19]  Finn A. GENnS.  Distribution of Acetyl Cholinesterase in the Hippocampal Region of the Guinea Pig , 1972 .

[20]  M. Colonnier,et al.  Thalamic projections of the superior colliculus in the rhesus monkey, Macaca mulatta. A light and electron microscopic study , 1977, The Journal of comparative neurology.

[21]  W. C. Hall,et al.  Connections of the visual cortex in the hedgehog (Paraechinus hypomelas). I. Thalamocortical projections. , 1978, The Journal of comparative neurology.

[22]  A. L. Humphrey,et al.  Laminar organization of receptive-field properties in tree shrew superior colliculus. , 1978, Journal of neurophysiology.

[23]  J. Kaas,et al.  Cortical connections of the visual pulvinar complex in prosimian galagos (Otolemur garnetti) , 2009, The Journal of comparative neurology.

[24]  J. Kaas,et al.  The Primate visual system , 2003 .

[25]  J. Tigges.  Retinal projections to subcortical optic nuclei in diurnal and nocturnal squirrels. , 1970, Brain, behavior and evolution.

[26]  R. Mize,et al.  Contour discrimination in the rat following removal of posterior neocortex. , 1971, Physiology & behavior.

[27]  J. Kaas,et al.  Architectonic Subdivisions of Neocortex in the Gray Squirrel (Sciurus carolinensis) , 2008, Anatomical record.

[28]  W. C. Hall,et al.  Cortical visual areas in the grey squirrel (Sciurus carolinesis): a correlation between cortical evoked potential maps and architectonic subdivisions. , 1971, Journal of neurophysiology.

[29]  J. Kaas,et al.  Thalamic connections of architectonic subdivisions of temporal cortex in grey squirrels (Sciurus carolinensis) , 2008, The Journal of comparative neurology.

[30]  J. Kaas,et al.  The inferior pulvinar complex in owl monkeys: Architectonic subdivisions and patterns of input from the superior colliculus and subdivisions of visual cortex , 1979, The Journal of comparative neurology.

[31]  C. R. Michael,et al.  Functional organization of cells in superior colliculus of the ground squirrel. , 1972, Journal of neurophysiology.

[32]  Iwona Stepniewska,et al.  The Pulvinar Complex , 2003 .

[33]  W. C. Hall,et al.  The organization of the pulvinar in the grey squirrel (Sciurus carolinensis). I. Cytoarchitecture and connections , 1977, The Journal of comparative neurology.

[34]  V. Casagrande,et al.  The projection of the primate superior colliculus upon the dorsal lateral geniculate nucleus: autoradiographic demonstration of interlaminar distribution of tectogeniculate axons , 1978, Brain Research.

[35]  M. Wong-Riley.  Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry , 1979, Brain Research.

[36]  J. Kaas,et al.  Architectonic subdivisions of the inferior pulvinar in New World and Old World monkeys , 1997, Visual Neuroscience.

[37]  M. Umemiya,et al.  A Calcium-Dependent Feedback Mechanism Participates in Shaping Single NMDA Miniature EPSCs , 2001, The Journal of Neuroscience.

[38]  J. K. Harting,et al.  Sublamination within the superficial gray layer of the squirrel monkey: an analysis of the tectopulvinar projection using anterograde and retrograde transport methods , 1983, Brain Research.

[39]  I. T. Diamond,et al.  The Organization and Function of the Visual Cortex in the Tree Shrew; pp. 244–263 , 1968 .

[40]  R. Kuljiš,et al.  On the organization of the retino-tecto-thalamo-telencephalic pathways in a Chilean rodent; theOctodon degus , 1982, Brain Research.

[41]  Jon H. Kaas,et al.  Variability in the sizes of brain parts , 2001, Behavioral and Brain Sciences.

[42]  H Sherk,et al.  Connections and visual-field mapping in cat's tectoparabigeminal circuit. , 1979, Journal of neurophysiology.

[43]  R W Guillery,et al.  Some principles of organization in the dorsal lateral geniculate nucleus. , 1972, Brain, behavior and evolution.

[44]  Iwona Stepniewska,et al.  Thalamocortical connections of functional zones in posterior parietal cortex and frontal cortex motor regions in New World monkeys. , 2010, Cerebral cortex.

[45]  J. Kaas,et al.  Retinal projections in adult and newborn grey squirrels. , 1982, Brain research.

[46]  J. Chaline.  Rodents, evolution, and prehistory , 1977 .

[47]  G. Jeffery,et al.  Subcortical afferent and efferent connections of the superior colliculus in the rat and comparisons between albino and pigmented strains , 2004, Experimental Brain Research.

[48]  L. Benevento,et al.  The organization of projections of the retinorecipient and nonretinorecipient nuclei of the pretectal complex and layers of the superior colliculus to the lateral pulvinar and medial pulvinar in the macaque monkey , 1983, The Journal of comparative neurology.

[49]  W. C. Hall,et al.  Projections from the superior colliculus to the dorsal lateral geniculate nucleus of the grey squirrel (Sciurus carolinensis) , 1976, Brain Research.

[50]  Edward M. Callaway,et al.  A Disynaptic Relay from Superior Colliculus to Dorsal Stream Visual Cortex in Macaque Monkey , 2010, Neuron.

[51]  J. Kaas,et al.  Convergences in the Modular and Areal Organization of the Forebrain of Mammals: Implications for the Reconstruction of Forebrain Evolution , 2002, Brain, Behavior and Evolution.

[52]  W. C. Hall,et al.  Evolution of the primate visual system: anterograde degeneration studies of the tecto-pulvinar system. , 1973, American journal of physical anthropology.

[53]  Jon H Kaas,et al.  Architectonic Subdivisions of Neocortex in the Tree Shrew (Tupaia belangeri) , 2009, Anatomical record.

[54]  M. Bickford,et al.  Synaptic organization of the tectorecipient zone of the rat lateral posterior nucleus , 2009, The Journal of comparative neurology.

[55]  W. C. Hall,et al.  The pulvinar nucleus of Galago senegalensis , 1975, The Journal of comparative neurology.

[56]  M. Paolini,et al.  Direction selectivity in the middle lateral and lateral (ML and L) visual areas in the California ground squirrel. , 1998, Cerebral cortex.

[57]  Troy A. Hackett,et al.  Regional and laminar distribution of the vesicular glutamate transporter, VGluT2, in the macaque monkey auditory cortex , 2009, Journal of Chemical Neuroanatomy.

[58]  J. Jane,et al.  Effects of visual cortical ablation on pattern discrimination in the ground squirrel (Citellus tridecemlineatus). , 1973, Experimental neurology.

[59]  B. Giros,et al.  The Existence of a Second Vesicular Glutamate Transporter Specifies Subpopulations of Glutamatergic Neurons , 2001, The Journal of Neuroscience.

[60]  P. Abplanalp.  Some subcortical connections of the visual system in tree shrews and squirrels. , 1970, Brain, behavior and evolution.

[61]  Terry T. Takahashi,et al.  The organization of the lateral thalamus of the hooded rat , 1985, The Journal of comparative neurology.

[62]  W. Murphy,et al.  Resolution of the Early Placental Mammal Radiation Using Bayesian Phylogenetics , 2001, Science.

[63]  D. B. Bender,et al.  Bilateral projections from the parabigeminal nucleus to the superior colliculus in monkey , 2004, Experimental Brain Research.

[64]  W. C. Hall,et al.  Course and laminar origin of the tectoparabigeminal pathway , 1981, Brain Research.

[65]  M. Bickford,et al.  Ultrastructural examination of diffuse and specific tectopulvinar projections in the tree shrew , 2008, The Journal of comparative neurology.

[66]  E. Wagor.  Pattern vision in the grey squirrel after visual cortex ablation. , 1978, Behavioral biology.

[67]  J. K. Harting,et al.  Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: Organization of tectogeniculate pathways in nineteen species , 1991, The Journal of comparative neurology.

[68]  J. Buettner‐Janusch.  The Antecedents of Man , 1963, The Yale Journal of Biology and Medicine.

[69]  J. Kaas,et al.  Projections of the superior colliculus to subdivisions of the inferior pulvinar in New World and Old World monkeys , 2000, Visual Neuroscience.

[70]  Béatrice de Gelder,et al.  Collicular Vision Guides Nonconscious Behavior , 2010, Journal of Cognitive Neuroscience.

[71]  C. Blakemore,et al.  Projections to the visual cortex in the golden hamster , 1979, The Journal of comparative neurology.

[72]  V. Casagrande,et al.  A light microscopic and electron microscopic study of the superficial layers of the superior colliculus of the tree shrew (Tupaia glis) , 1980, The Journal of comparative neurology.

[73]  I. T. Diamond.  Organization of the visual cortex: comparative anatomical and behavioral studies. , 1976, Federation proceedings.

[74]  W. C. Hall,et al.  Visual cortex of the grey squirrel (Sciurus carolinensis): Architectonic subdivisions and connections from the visual thalamus , 1972, The Journal of comparative neurology.

[75]  R. Held,et al.  Residual Visual Function after Brain Wounds involving the Central Visual Pathways in Man , 1973, Nature.

[76]  Shigeyoshi Higo,et al.  Ascending projections from the nucleus of the brachium of the inferior colliculus in the cat , 2004, Experimental Brain Research.

[77]  Thalamic connections of the ground squirrel superior colliculus and their topographic relations. , 1988, Journal fur Hirnforschung.

[78]  Jon H. Kaas,et al.  Pulvinar contributions to the dorsal and ventral streams of visual processing in primates , 2007, Brain Research Reviews.

[79]  J. T. Weber,et al.  Chemoarchitectonic subdivisions of the visual pulvinar in monkeys and their connectional relations with the middle temporal and rostral dorsolateral visual areas, MT and DLr , 1993, The Journal of comparative neurology.

[80]  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.

[81]  G. Schneider,et al.  Afferents from the colliculus, cortex, and retina have distinct terminal morphologies in the lateral posterior thalamic nucleus , 1997, The Journal of comparative neurology.

[82]  David C Lyon,et al.  The visual pulvinar in tree shrews II. Projections of four nuclei to areas of visual cortex , 2003, The Journal of comparative neurology.

[83]  M. Bickford,et al.  Synaptic organization of connections between the temporal cortex and pulvinar nucleus of the tree shrew. , 2010, Cerebral cortex.

[84]  H. Karten,et al.  Bottlebrush dendritic endings and large dendritic fields: Motion‐detecting neurons in the mammalian tectum , 2000, The Journal of comparative neurology.

[85]  F. Reinoso-suárez,et al.  Parabigeminal projections to the superior colliculus in the cat , 1983, Brain Research.

[86]  W. C. Hall,et al.  Organization of the intermediate gray layer of the superior colliculus. I. Intrinsic vertical connections. , 2004, Journal of neurophysiology.