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

Abstract

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.

Prefrontal Projections to the Thalamic Reticular Nucleus form a Unique Circuit for Attentional Mechanisms

“…In a few occasions, large boutons branching out from the latter axons formed aggregated clusters, resembling bunches of grapes, as described for sensory cortical projections in several other thalamic nuclei but not TRN (Ojima, 1994;Bourassa et al, 1995;Ojima et al, 1996). Some axons with large en passant boutons formed round arbors at the termination sites, similar to those described for corticopulvinar projections (Rockland, 1996). The rest of the axonal branches (29%) gave rise to a mixture of small and large boutons.…”

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).…”

Spikes, synchrony, and attentive learning by laminar thalamocortical circuits

“…In the primate, synaptic terminals in the thalamus can be roughly subdivided into two classes (Rockland, 1996;Sherman and Guillery, 2001): (a) round-large (RL) synapses, such as retinogeniculate synapses. These synapses are believed to be driving; (b) round-small (RS) terminations, such as the corticothalamic synapses from V1 layer 6 to the LGN.…”