Retinal projections to the inferior and medial pulvinar nuclei in the old-world monkey

Itaya, Stephen K.; Hoesen, Gary W. Van

doi:10.1016/0006-8993(83)90131-2

Cited by 71 publications

(34 citation statements)

References 48 publications

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“…The rostral projection of retinal fibers over the dorsal thalamus was originally described in the tree shrew by Conrad and Stumpf (1975) and was later observed in monkeys (Itaya and Van Hoesen, 1983;Nakagawa and Tanaka, 1984). Conrad and Stumpf (1975) reported that this fiber bundle originated in the vicinity of the LGN and terminated in the anterodorsal thalamic nucleus, but other studies, including the present study, have not clearly labeled the terminal field of this "retinalanterodorsal" tract.…”

Section: "Retinal-anterodorsal" Tractmentioning

confidence: 48%

Pattern of retinal projections in the California ground squirrel (Spermophilus beecheyi): Anterograde tracing study using cholera toxin

Major

Rodman

Libedinsky

et al. 2003

J of Comparative Neurology

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The retinofugal pathways in the California ground squirrel, Spermophilus beecheyi, were mapped after intravitreal injections of cholera toxin B-subunit. The results of the current study are consistent with work in other mammals and provide new details relevant to the organization and evolution of the visual system. All retinorecipient nuclei received bilateral input, with a contralateral predominance. The suprachiasmatic nucleus is heavily innervated, and sparse terminals were noted in other hypothalamic areas. In addition to the interstitial, medial, lateral, and dorsal terminal nuclei, a few fibers of the accessory optic tract may enter the ventral lateral geniculate and the nucleus of the optic tract, though this innervation may not derive from the same ganglion cells innervating the accessory optic nuclei. Retinal terminals are found in the intergeniculate leaflet and the "dorsal cap" of the ventral lateral geniculate. Retinal fibers pass rostrally from the dorsal cap toward the anterodorsal thalamus, confirming a projection described in the tree shrew and monkeys. Retinal termination patterns in the dorsal lateral geniculate reveal a hexilaminate organization of alternating ipsilateral and contralateral input. Variations in terminal morphology suggest that sublayers receive input from distinct ganglion cell types and that laminar comparisons can be made with primates. Finally, terminal patterns in the superior colliculus reveal a dense, highly ordered columnar organization supporting functional properties of tectal receptive fields. All the visual structures in the ground squirrel are large and well differentiated, making the sciurid visual system an accessible rodent model for comparing visual processing with that in other diurnal vertebrates.

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Section: "Retinal-anterodorsal" Tractmentioning

confidence: 48%

Pattern of retinal projections in the California ground squirrel (Spermophilus beecheyi): Anterograde tracing study using cholera toxin

Major

Rodman

Libedinsky

et al. 2003

J of Comparative Neurology

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“…Even today, deadly interactions with snakes are best avoided with early detection and a shifting of attention to them. The medial pulvinar receives direct inputs from the retina (13,18) and the deeper layers of the superior colliculus (15,19). Although the superior colliculus is considered a visual structure, it is also involved in threat-relevant motor behavior.…”

Section: Discussionmentioning

confidence: 99%

Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes

Isbell

Matsumoto

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

229

157

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Snakes and their relationships with humans and other primates have attracted broad attention from multiple fields of study, but not, surprisingly, from neuroscience, despite the involvement of the visual system and strong behavioral and physiological evidence that humans and other primates can detect snakes faster than innocuous objects. Here, we report the existence of neurons in the primate medial and dorsolateral pulvinar that respond selectively to visual images of snakes. Compared with three other categories of stimuli (monkey faces, monkey hands, and geometrical shapes), snakes elicited the strongest, fastest responses, and the responses were not reduced by low spatial filtering. These findings integrate neuroscience with evolutionary biology, anthropology, psychology, herpetology, and primatology by identifying a neurobiological basis for primates' heightened visual sensitivity to snakes, and adding a crucial component to the growing evolutionary perspective that snakes have long shaped our primate lineage.evolution | Snake Detection Theory | visual responses | low-pass filtered images S nakes have long been of interest to us above and beyond the attention we give to other wild animals. The attributes of snakes and our relationships with them have been topics of discussion in fields as disparate as religion, philosophy, anthropology, psychology, primatology, and herpetology (1, 2). Ochre and eggshells dated to as early as 75,000 y ago and found with cross-hatched and ladder-shaped lines (3, 4) resemble the dorsal and ventral scale patterns of snakes. As the only natural objects with those characteristics, snakes may have been among the first models used in representational imagery created by modern humans. Our interest in snakes may have originated much further back in time; our primate lineage has had a long and complex evolutionary history with snakes as competitors, predators, and prey (1). The position of primates as prey of snakes has, in fact, been argued to have constituted strong selection favoring the evolution of the ability to detect snakes quickly as a means of avoiding them, beginning with the earliest primates (2, 5). Across primate species, ages, and (human) cultures, snakes are indeed detected visually more quickly than innocuous stimuli, even in cluttered scenes (6-11). Physiological responses reveal that humans are also able to detect snakes visually even before becoming consciously aware of them (12). Although the visual system must be involved in the preferential ability to detect snakes rapidly and preconsciously or automatically, the neurological basis for this ability has not yet been elucidated, perhaps because an evolutionary perspective is rarely incorporated in neuroscientific studies. Our study helps to fill this interdisciplinary gap by investigating the responses of neurons to snakes and other natural stimuli that may have acted as selective pressures on primates in the past.Here, we identify a mechanism for the visual system's involvement in rapid snake detection by measurin...

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“…Besides visual cortical inputs, parts of PI, PL, and PM receive connections from the retina (Itaya and Van Hoesen, 1983;Cowey et al, 1994) and superior colliculus (Benevento and Fallon, 1975;Benevento and Standage, 1983;Lysakowski et al, 1986). PM, in addition receives widespread cortical input from cingulate and frontal areas and connections from the amygdala (Baleydier and Mauguiere, 1985;Kaas and Huerta, 1988;Robinson and Cowie, 1996).…”

Section: ! Imentioning

confidence: 99%

Two types of corticopulvinar terminations: Round (type 2) and elongate (type 1)

Rockland

1996

J. Comp. Neurol.

116

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Corticopulvinar axons were anterogradely labeled by Phaseolus vulgaris-leucoagglutinin injections in the occipitotemporal cortex of the macaque to determine quantitative parameters of divergence and convergence, arbor size and shape, and distribution of terminal specializations. Forty individual axons were analyzed by serial section reconstruction and divided into two major groups. The majority of axons have numerous (typically 500-1,000) small, spinous endings (boutons terminaux). These axons have terminal fields that are beam-like or elongated (E, corresponding to classical type 1) and highly divergent (1.0-3.0 mm). These frequently innervate several of the traditionally designated pulvinar subdivisions; namely inferior pulvinar (PI) and the ventral part of interal pulvinar (PL); medial pulvinar (PM) and dorsal PL, and (one axon) PM, dorsal PL, and PI. Some axons, however (R or round, corresponding to classical type 2), have a small number (typically 70-160) of primarily large, beaded endings (boutons en passant), which concentrate in sharply delimited, round arbors (diameters 100-125 microns). R axons appear to be larger caliber than E axons (1.0-1.5 microns vs. 0.5-1.0 micron, respectively). These differences in phenotype are probably associated with distinct types of projection neurons. In visual areas, corticopulvinar terminations are reported to originate from pyramidal cell subpopulations in layer 5. Indirect evidence, presented here, suggests that the more numerous medium-sized neurons give rise to E axons, and the sparser giant pyramids give rise to R corticopulvinar axons. If this is correct, corticopulvinar connectivity may be involved in multiple transformations. Spatially, axons of giant neurons (with basal dendrites that collect intracortically from a disc-like area, about 1.0 mm in diameter) converge onto a small number of pulvinar neurons. Axons of medium neurons (with basal dendrites that occupy a small intracortical disc, about 0.3 mm in diameter) diverge over 1.0-3.0 mm in the pulvinar and may form many contacts. Giant neurons, although numerically few in relation to medium pyramids (1 or 2: 50?), are likely to have distinctive membrane properties (functionally equivalent to bursting neurons?). Their larger boutons and axon caliber may be associated with a faster transmission that compensates for their small numbers. In primates, the E and R duality does not characterize cortical projections to the caudate, lateral geniculate nucleus, pons, or superior colliculus and thus may be essentially linked to pulvinar-specific processes.

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Retinal projections to the inferior and medial pulvinar nuclei in the old-world monkey

Cited by 71 publications

References 48 publications

Pattern of retinal projections in the California ground squirrel (Spermophilus beecheyi): Anterograde tracing study using cholera toxin

Pattern of retinal projections in the California ground squirrel (Spermophilus beecheyi): Anterograde tracing study using cholera toxin

Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes

Two types of corticopulvinar terminations: Round (type 2) and elongate (type 1)

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