Connections of higher order visual relays in the thalamus: A study of corticothalamic pathways in cats

Abstract

Axonal markers injected into layers 5 and 6 of cortical areas 17, 18, or 19 labeled axons going to the lateral geniculate nucleus (LGN), the lateral part of the lateralis posterior nucleus (LPl), and pulvinar (P). Area 19 sends fine axons (type 1, Guillery [1966] J Comp Neurol 128:21-50) to LGN, LPl, and P, and thicker, type 2 axons to LPl and P. Areas 17 and 18 send type 1 axons to LGN, and a few type 1, but mainly type 2 axons to LPl and P. Type 1 and 2 axons from a single small cortical locus distribute to distinct, generally nonoverlapping parts of LP and P; type 1 axons have a broader distribution than type 2 axons. Type 2 axons, putative drivers of thalamic relay cells (Sherman and Guillery [1998] Proc Natl Acad Sci USA 95:7121-7126; Sherman and Guillery [2001] Exploring the thalamus. San Diego: Academic Press), supply small terminal arbors (100- to 200-microm diameter) in LPl and P, and then continue into the midbrain. Each thalamic type 2 arbor contains two terminal types. One, at the center of the arbor, is complex and multilobulated; the other, with a more peripheral distribution, is simpler and may contribute to adjacent arbors. Type 2 arbors from a single injection are scattered around and along "isocortical columns" in LPl, (i.e., columns that represent cells having connections to a common cortical locus). Evidence is presented that the connections and consequently the functional properties of cells in LP change along these isocortical columns. Type 2 driver afferents from a single cortical locus can, thus, be seen as representing functionally distinct, parallel pathways from cortex to thalamus.

Distribution, morphology, and synaptic targets of corticothalamic terminals in the cat lateral posterior-pulvinar complex that originate from the posteromedial lateral suprasylvian cortex

“…Alternatively, the visual activity in the LPl that remains when area 17 is silenced may be contributed by projections from areas 18, 19, or 21a. These areas all innervate the LPl (Updyke, 1977(Updyke, , 1986Berson and Graybiel, 1983), and the projections from areas 18 and 19 have been shown to exhibit type II morphology (Ojima et al, 1996;Guillery et al, 2001). In addition, the LPl receives direct input from the retina (Boire et al, 2004).…”

“…2B-D). In the nomenclature of Guillery et al (2001), these terminals were classified as singletons. Two larger terminal types formed more complex endings.…”

Ultrastructural analysis of projections to the pulvinar nucleus of the cat. I: Middle suprasylvian gyrus (areas 5 and 7)

“…It has been suggested recently that the cortex may provide the primary or driving input to higher order nuclei, such as the PUL and lateral posterior nucleus (LP; Guillery, 1995;Guillery et al, 2001). This is based on the observation that terminals in the LP originating from layer V of the striate cortex are similar in morphology (RL profiles, denoting large terminals that contain round vesicles) to retinal terminals in the dorsal lateral geniculate nucleus (dLGN; Vidnyánszky et al, 1996;Feig and Harting, 1998).…”

“…Neurons located in this region were originally described as polysensory (Amassian, 1954); although later studies indicated that neurons within this region could be categorized primarily based on their responses to visual stimuli, including stationary spots, brisk movements, and oriented edges (Thompson et al, 1963; Dubner, 1969, 1971;Robertson et al, 1975; Yin and Greenwood, 1992a,b). More recently, visual, saccade, and fixational responses were distinguished within more caudal portions of the MSg (Yin and Greenwood, 1992b).It has been suggested recently that the cortex may provide the primary or driving input to higher order nuclei, such as the PUL and lateral posterior nucleus (LP; Guillery, 1995;Guillery et al, 2001). This is based on the observation that terminals in the LP originating from layer V of the striate cortex are similar in morphology (RL profiles, denoting large terminals that contain round vesicles) to retinal terminals in the dorsal lateral geniculate nucleus (dLGN; Vidnyánszky et al, 1996;Feig and Harting, 1998).…”

Fewer driver synapses in higher order than in first order thalamic relays

“…Examples of these higher order relays are the pulvinar for vision, the posterior nucleus for somesthesia, and the magnocellular portion of the medial geniculate nucleus for hearing (Sherman andGuillery, 1996, 2006;Sherman, 2005). Central to this view is evidence showing that synaptic properties of corticothalamic input from layer 5 to higher order nuclei share the same driver properties measured anatomically, physiologically, and pharmacologically as do retinogeniculate input and medial lemniscal input to the ventral posterior nucleus (Schwartz et al, 1991;Hoogland et al, 1991;Deschênes et al, 1994;Ojima, 1994;Rockland, 1996;Rouiller and Welker, 2000;Bartlett et al, 2000;Guillery et al, 2001;Li et al, 2003b;Reichova and Sherman, 2004). These higher order relays have only been recently recognized, and they seem to occupy the majority of thalamus (Sherman and Guillery, 2006).…”