The afferent and efferent organization of the lateral geniculo‐prestriate pathways in the macaque monkey

Both anterograde (autoradiographic) and retrograde (horseradish peroxidase) tracing techniques were used to identify and characterize projections from the dorsal lateral geniculate nucleus (DLG) of the thalamus to the subdivisions of occipital prestriate cortex (generally defined by areas 18 and 19) in macaque monkeys. It was found that the DLG projects to area 19 and the anterior portion of area 18 located on the lateral, ventral, and ventromedial surfaces of the hemisphere. There is a general topographical organization such that the medial portion of the DLG projects to dorsal prestriate located between the lunate and superior temporal sulci, while the lateral portion of the DLG projects to ventral prestriate extending from the inferior occipitotemporal sulcus. In contrast DLG inputs to the lunate, superior temporal, and inferior occipital sulci are limited in extent, and involve only a portion of the bank or shoulder of each sulcus which is continuous with the cortex located on the surfaces of the surrounding preoccipital gyri. The projection to the inferior occipital sulcus is more extensive than the ones to the lunate and superior temporal sulci and involves the floor as well as the ventral bank. This means that there are certain functional subdivisions, such as those located within the lunate (eg, visual area 2) and superior temporal sulici which do not receive DLG input. Regardless of the location of these projections the terminal pattern was the same and occurred in horizontally segregated “patches” which were restricted to layer V and the lower, adjacent portion of layer IV. In contrast, the projections from the nearby pulvinar to cortical layers IV, III, and I of the same prestriate areas do not overlap with those from the DLG. An attempt was made to identify possible afferent inputs to these DLG‐prestriate paths. The HRP experiments reveal that the DL‐Gprestriate cells are concentrated in the DLG interlaminar zones and that their distribution overlaps the distribution of terminals from the superior colliculus and, as shown previously, prestriate cortex. Intraocular injections of radioactive precursors demonstrated transsynaptic transport to a number of structures except prestriate cortex. While the latter result does not prove that the DLG‐prestriate cells do not receive retinal input, one conclusion is that the DLG‐prestriate projection could be organized like pulvino‐prestriate systems which receive their inputs from the midbrain and cortex.

[1]  H. Hughes,et al.  Anatomical and neurobehavioral investigations concerning the thalamo‐cortical organization of the rat's visual system , 1977, The Journal of comparative neurology.

[2]  L. Benevento,et al.  A comparison of the organization of the projections of the dorsal lateral geniculate nucleus, the inferior pulvinar and adjacent lateral pulvinar to primary visual cortex (area 17) in the macaque monkey , 1979, Brain Research.

[3]  A. Hendrickson,et al.  Neuronal and synaptic structure of the dorsal lateral geniculate nucleus in normal and monocularly deprived Macaca monkeys , 1981, The Journal of comparative neurology.

[4]  J Miller,et al.  Visual responses of single neurons in the caudal lateral pulvinar of the macaque monkey , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  J. Kaas,et al.  Projections from cortical visual areas 17, 18, and MT onto the dorsal lateral geniculate nucleus in owl monkeys , 1977, The Journal of comparative neurology.

[6]  Masao Yukie,et al.  A quantative study of the cells projecting from the lateral geniculate nucleus to the prestriate cortex in the monkey with horseradish peroxidase , 1979, Neuroscience Letters.

[7]  E. Geisert,et al.  Cortical projections of the lateral geniculate nucleus in the cat , 1980, The Journal of comparative neurology.

[8]  L. Benevento,et al.  The cortical projections of the inferior pulvinar and adjacent lateral pulvinar in the rhesus monkey (macaca mulatta): An autoradiographic study , 1976, Brain Research.

[9]  P. Schiller,et al.  Properties and tectal projections of monkey retinal ganglion cells. , 1977, Journal of neurophysiology.

[10]  M. Mesulam,et al.  The blue reaction product in horseradish peroxidase neurohistochemistry: incubation parameters and visibility. , 1976, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[11]  R. Marrocco,et al.  Correlation of receptive field properties of monkey LGN cells with the conduction velocity of retinal afferent input , 1975, Brain Research.

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

[13]  Margaret T. T. Wong-Riley,et al.  Projections from the dorsal lateral geniculate nucleus to prestriate cortex in the squirrel monkey as demonstrated by retrograde transport of horseradish peroxidase , 1976, Brain Research.

[14]  J. Kaas,et al.  Projections from the pulvinar to the middle temporal visual area (MT) in the owl monkey, Aotus trivirgatus. , 1974, Brain research.

[15]  J. Stone,et al.  Very slow-conducting ganglion cells in the cat's retina: a major, new functional type? , 1972, Brain research.

[16]  F. Ebner,et al.  The contribution of the dorsal lateral geniculate nucleus to the total pattern of thalamic terminations in striate cortex of the virginia opossum , 1971, The Journal of comparative neurology.

[17]  J. Stone,et al.  Projection of X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of visual cortex. , 1973, Journal of neurophysiology.

[18]  D H Hubel,et al.  Autoradiographic demonstration of ocular-dominance columns in the monkey striate cortex by means of transneuronal transport. , 1974, Brain research.

[19]  L. Benevento,et al.  An autoradiographic study of the projections of the pretectum in the rhesus monkey (macaca mulatta): evidence for sensorimotor links to the thalamus and oculomotor nuclei , 1977, Brain Research.

[20]  M. Berkley,et al.  Cortical projections from the dorsal lateral geniculate nucleus of cats , 1967, The Journal of comparative neurology.

[21]  L. Benevento,et al.  The ascending projections of the superior colliculus in the rhesus monkey (Macaca mulatta) , 1975, The Journal of comparative neurology.

[22]  S. Zeki.  Functional specialisation in the visual cortex of the rhesus monkey , 1978, Nature.

[23]  Michael H. Rowe,et al.  Some observations on the patterns of segregated geniculate inputs to the visual cortex in New World primates: an autoradiographic study , 1978, Brain Research.

[24]  Richard T. Marrocco,et al.  Binocular interaction in the lateral geniculate nucleus of the monkey , 1979, Brain Research.

[25]  W. C. Hall,et al.  Evolution of neocortex. , 1969, Science.

[26]  C. Enroth-Cugell,et al.  The contrast sensitivity of retinal ganglion cells of the cat , 1966, The Journal of physiology.

[27]  L. Benevento,et al.  Extrageniculate thalamic projections to the primary visual cortex , 1980, Brain Research.

[28]  K. Yoshida,et al.  The projection from the dorsal lateral geniculate nucleus of the thalamus to extrastriate visual association cortex in the macaque monkey , 1981, Neuroscience Letters.

[29]  W. C. Hall,et al.  Laminar origin of projections from the superficial layers of the superior colliculus in the tree shrew, Tupaia glis , 1979, Brain Research.

[30]  W. Hayhow,et al.  The Organization of the Thalamo-Cortical Visual Pathways in the Cat; pp. 220–237 , 1971 .

[31]  C. Gilbert,et al.  Laminar patterns of geniculocortical projection in the cat , 1976, Brain Research.

[32]  L. Palmer,et al.  An autoradiographic study of the projections of the dorsal lateral geniculate nucleus and the posterior nucleus in the cat. , 1974, Brain research.

[33]  M. Ogren,et al.  The neurological organization of pathways between the dorsal lateral geniculate nucleus and visual cortex in old world and new world primates , 1978, The Journal of comparative neurology.

[34]  T. Powell,et al.  An experimental study of the termination of the lateral geniculo–cortical pathway in the cat and monkey , 1971, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[35]  R. Giolli,et al.  Visual thalamocortical connections in sheep studied by means of the retrograde transport of Horseradish‐Peroxidase , 1979, The Journal of comparative neurology.

[36]  A. Hendrickson,et al.  The distribution of pulvinar terminals in visual areas 17 and 18 of the monkey , 1977, Brain Research.

[37]  L. Benevento,et al.  Demonstration of a direct projection from the intralaminar central lateral nucleus to the primary visual cortex , 1979, Neuroscience Letters.

[38]  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.

[39]  L. Benevento,et al.  Extrageniculate projections to layers VI and I of striate cortex (area 17) in the rhesus monkey (Macaca mulatta) , 1975, Brain Research.

[40]  A. Hendrickson,et al.  The autoradiographic demonstration of axonal connections in the central nervous system. , 1972, Brain research.

[41]  S Zeki,et al.  A direct projection from area V1 to area V3A of rhesus monkey visual cortex , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[42]  J. Tigges,et al.  Complementary laminar terminations of afferents to area 17 originating in area 18 and in the lateral geniculate nucleus in squirrel monkey , 1977, The Journal of comparative neurology.

[43]  Richard T. Marrocco,et al.  Conduction velocities of afferent input to superior colliculus in normal and decorticate monkeys , 1978, Brain Research.

[44]  D. Hubel,et al.  Laminar and columnar distribution of geniculo‐cortical fibers in the macaque monkey , 1972, The Journal of comparative neurology.

[45]  R. W. Rodieck,et al.  Identification, classification and anatomical segregation of cells with X‐like and Y‐like properties in the lateral geniculate nucleus of old‐world primates. , 1976, The Journal of physiology.