Corticocortical communication via the thalamus: Ultrastructural studies of corticothalamic projections from area 17 to the lateral posterior nucleus of the cat and inferior pulvinar nucleus of the owl monkey

Abstract

Electron microscopic anterograde autoradiography has been used to analyze the morphology and postsynaptic relationships of area 17 cortical terminals in the lateral division of the lateral posterior nucleus (LPl) of the cat and medial division of the inferior pulvinar nucleus (IPm) of the owl monkey. Such terminals are thought to arise exclusively from layer 5 in the cat and primate (Lund et al. [1975] J. Comp. Neurol. 164:287-304; Abramson and Chalupa [1985] Neuroscience 15:81-95). All labeled terminals in both nuclei exhibited the morphology of ascending "lemniscal" afferents. That is, they contained round vesicles, were large, made asymmetrical synaptic and filamentous nonsynaptic contacts, and were classified as RLs. These cortical RLs also exhibited the postsynaptic relationships of lemniscal afferents. Thus, they were presynaptic to large dendrites within glial encapsulated glomeruli, where a majority was involved in complex synaptic arrangements called triads. They also were found adjacent to terminal profiles with pleomorphic vesicles but never adjacent to small terminals containing round vesicles. Our results suggest that the layer 5 projection from area 17 provides a functional "drive" for some LPl and IPm neurons. Information carried over this "re-entrant" pathway (Guillery [1995] J. Anat. 187:583-592) could be modified within the LPl and IPm by both cortical and subcortical pathways and subsequently conveyed to higher visual cortical areas, where it could be integrated with messages carried through the well-documented corticocortical pathways (Casagrande and Kaas [1994] Cerebral cortex New York: Plenum Press).

Multisensory anatomical pathways

“…Such feedforward corticothalamic projections with giant endings have been demonstrated for many sensory and motor cortical areas (e.g. Darian-Smith et al, 1999;Ojima, 1994;Rockland, 1996;Rouiller and Durif, 2004;Rouiller et al, 1998Rouiller et al, , 2003Schwartz et al, 1991;Taktakishvili et al, 2002;Cappe et al, 2007a), representing an anatomical support for fast interactions between distant cortical regions, via the thalamus (see also Feig and Harting, 1998;Sherman and Guillery, 2002;Van Horn and Sherman, 2004). Such cortico-thalamo-cortical routing is thus suitable for multisensory interplay by a convergence of different modalities on the same thalamic nucleus that then in turn makes this integrated information available to a target cortical region, for instance the premotor cortex (PM) or the prefrontal cortex (Pf).…”

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

“…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). Because RL profiles have been observed in the PUL (Majorossy et al, 1965;Baldauf et al, 2003), the similarities in the response properties of PUL neurons and parietal cortex neurons could be due to a driving influence of cortical projections to the PUL.…”

“…In the cat striate cortex, corticogeniculate neurons are restricted to layer VI (Gilbert and Kelly, 1975), and innervate the dLGN with thin (type I) axons and RS terminals that primarily make simple axodendritic synaptic contacts on the distal dendrites of thalamocortical cells (Vidnyánszky and Hámori, 1994;Paré and Smith, 1996;Eriºir et al, 1997). In contrast, striate cortico-LP cells are confined to layer V (Abramson and Chalupa, 1985) and innervate the LPl with thick (type II) axons and RL terminals that participate in complex glomerular synaptic arrangements in which they contact approximately equal numbers of thalamocortical cell and interneuron dendrites (Parê and Smith, 1996;Vidnyánszky et al, 1996;Feig and Harting, 1998;Baldauf et al, 2003;Kelly et al, 2003). Because the synaptic arrangements of RL corticothalamic terminals resemble those of retinogeniculate terminals (Robson and Mason, 1979;Rapisardi and Miles, 1984;Wilson et al, 1984;Hamos et al, 1987;Li et al, 2003b), it has been suggested that their function may be similar.…”

Signal processing in the tectothalamic pathway.

“…The inputs from cortical layer V to the dorsal thalamus are similar to retinogeniculate terminals. They are large terminals that participate in complex synaptic arrangements known as glomeruli, and contact proximal dendrites (Vidnyanszky et al 1996;Eri~ir et al 1997;Feig and Harting 1998;Baldauf et al 2005). Similarities in the excitatory postsynaptic potentials (EPSPs) elicited by stimulation of layer V corticothalamic terminals or retinogeniculate terminals in vitro have also been noted (Turner and Salt 1998;Chen et al 2002;Reichova and Sherman 2004).…”