Ultrastructural examination of diffuse and specific tectopulvinar projections in the tree shrew

Abstract

Two pathways from the superior colliculus (SC) to the tree shrew pulvinar nucleus have been described, one in which the axons terminate in dense (or specific) patches and one in which the axon arbors are more diffusely organized J. . As predicted by Lyon et al. ([2003] J. Comp. Neurol. 467:593-606), we found that anterograde labeling of the diffuse tectopulvinar pathway terminated in the acetylcholinesterase (AChE)-rich dorsal pulvinar (Pd), whereas the specific pathway terminated in the AChE-poor central pulvinar (Pc). Injections of retrograde tracers in Pd labeled non-γ-aminobutyric acid (GABA)-ergic wide-field vertical cells located in the lower stratum griseum superficiale and stratum opticum of the medial SC, whereas injections in Pc labeled similar cells in more lateral regions. At the ultrastructural level, we found that tectopulvinar terminals in both Pd and Pc contact primarily non-GABAergic dendrites. When present, however, synaptic contacts on GABAergic profiles were observed more frequently in Pc (31% of all contacts) compared with Pd (16%). Terminals stained for the type 2 vesicular glutamate transporter, a potential marker of tectopulvinar terminals, also contacted more GABAergic profiles in Pc (19%) compared with Pd (4%). These results provide strong evidence for the division of the tree shrew pulvinar into two distinct tectorecipient zones. The potential functions of these pathways are discussed. J. Comp. Neurol. 510:24 -46, 2008. Indexing termssynapse; ultrastructure; GABA; pulvinar nucleus; superior colliculus; vesicular glutamate transporter; Tupaia belangeri Parallel visual pathways from the retina to the cortex, relayed via the dorsal lateral geniculate nucleus (dLGN), or the superior colliculus (SC) and pulvinar nucleus, likely serve distinct functions in the coding of form, movement, and spatial location signals. In the dLGN, further segregations of anatomically and physiologically distinct visual pathways have been identified and extensively characterized (Sherman, 1985). Likewise, studies in a variety of species have provided evidence for the existence of multiple pathways from the SC to the thalamus (May, 2006), although these pathways are largely uncharacterized, and their functions are unclear. The tree shrew, with its expanded tectopulvinar system, is good choice for studies of how pathways from the SC influence cortical activity via their projections to the pulvinar nucleus.In 1988, Luppino et al. labeled tectothalamic terminals in the tree shrew by placing small injections of axonal tracers in the SC and discovered that the pulvinar nucleus receives input *Correspondence to: Martha E. Bickford, Department of Anatomical Sciences and Neurobiology, University of Louisville, School of Medicine, 500 S. Preston St., Louisville, KY 40292. E-mail: martha.bickford@louisville.edu. We recently examined the synaptic organization of two tectorecipient zones of the cat thalamus (Kelly et al., 2003). We found that tectal terminals in the medial subdivision of the lateral posterior (LPm) ...

A hard-wired priority map in the superior colliculus shaped by asymmetric inhibitory circuitry

“…Indeed, this inhibitory circuit could contribute to the disengagement of attention at an initial location (usually more central/nasal) that precedes a shift of attention to a peripheral field (Posner 1980). In this case, the changes in excitability in the visuosensory layers would be transmitted to attentional circuits in the cortex via the ascending collicular projections through the thalamus (Chomsung et al 2008;Karten et al 1997) to mediate rapid shifts of attention to a new location and disengagement of attention from the current location. Consistent with these ideas, increased excitability of visuosensory neurons in the SC was recently reported in a rat model of attention deficit disorder (Clements et al 2014).…”

Circuits for active vision : parallel tectothalamocortical visual pathways in the mouse.

“…Similar examples of driver-like convergence illustrate the complexity of thalamic organization. The dorsal thalamus may be divided not only into "first order" (driven by ascending peripheral input) or "higher order" (driven by descending cortical input) nuclei (Guillery and Sherman, 2002), but also "second order" nuclei driven by convergent, ascending inputs (Kelly et al, 2003;Smith et al, 2007;Chomsung et al, 2008;Masterson et al, 2009Masterson et al, , 2010, or nuclei that contain unique combinations of ascending and descending driver-like inputs (Baldauf et al, 2005;Rovo et al, 2012;Groh et al, 2014). Such diversity may dramatically increase the computational capabilities of the thalamus, reflecting its essential roles in sensory, motor, and sensory-motor circuits.…”

“…As schematically illustrated in Figure 11, this homology is based to a large extent on commonalities in the projections of the superficial (visual) layers of the superior colliculus (SC), or optic tectum, to the primate pulvinar nucleus, rodent/carnivore LPN, and avian nucleus rotundus (Harting et al, 1973b;Robson and Hall, 1977;Berson and Graybiel, 1978;Mooney et al, 1984;Takahashi, 1985;Abramson and Chalupa, 1988;Luppino et al, 1988;Hutsler and Chalupa, 1991;Villeneuve and Casanova, 2003;Kelly et al, 2003;Chomsung et al, 2008;Masterson et al, 2009Masterson et al, , 2010Baldwin et al, 2011;Wei et al, 2011b;Fredes et al, 2012;Baldwin et al, 2013). Because of these similarities, we will refer to this region of the mouse thalamus as the pulvinar nucleus.…”

Morphological comparison of visual pathway projections to the temporal lobe from cortical area VI and the tectorecipient zone of the pulvinar nucleus in the tree shrew (Tupaia belangeri).

“…Seven tree shrews were used to investigate the distribution and morphology of the projections to the temporal lobe labeled by injections of BDA in two areas of the pulvinar, the dorsal pulvinar (PD) (3 tree shrews) and the central pulvinar (PC) (4 tree shrews). Several of these animals were also used for previous studies (Chomsung et al 2008. All methods were approved by the University of Louisville Animal Care and Use Committee and conform to the National Institutes of Health guidelines.…”

“…PD carries a representation of the upper half of the field of vision from the superior colliculus while PC carries a representation of the lower vision field (Chomsung et al 2008;Dang et al 2012). This matches data from Lyon et al (2003), where they also found that only PD in the pUlvinar nucleus projected to TP.…”