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

Abstract

The mammalian pulvinar nucleus (PUL) establishes heavy interconnections with the parietal lobe, but the precise nature of these connections is only partially understood. To examine the distribution of corticopulvinar cells in the cat, we injected the PUL with retrograde tracers. Corticopulvinar cells were located in layers V and VI of a wide variety of cortical areas, with a major concentration of cells in area 7. To examine the morphology and distribution of corticopulvinar terminals, we injected cortical areas 5 or 7 with anterograde tracers. The majority of corticopulvinar axons were thin fibers (type I) with numerous diffuse small boutons. Thicker (type II) axons with fewer, larger boutons were also present. Boutons of type II axons formed clusters within restricted regions of the PUL. We examined corticopulvinar terminals labeled from area 7 at the ultrastructural level in tissue stained for γ-aminobutyric acid (GABA). By correlating the size of the presynaptic and postsynaptic profiles, we were able to quantitatively divide the labeled terminals into two categories: small and large (RS and RL, respectively). The RS terminals predominantly innervated small-caliber non-GABAergic (thalamocortical cell) dendrites, whereas the RL terminals established complex synaptic arrangements with dendrites of both GABAergic interneurons and non-GABAergic cells. Interpretation of these results using Sherman and Guillery's recent theories of thalamic organization (Sherman and Guillery [1998] Proc Natl Acad Sci U S A 95:7121-7126) suggests that area 7 may both drive and modulate PUL activity. Indexing termscortex; thalamus; visual system; sensorimotor; ultrastructure The feline pulvinar nucleus (PUL) receives input from a wide array of cortical areas (Raczkowski and Rosenquist, 1983) as well as the pretectum (PT;Berman, 1977;Berson and Graybiel, 1978;Schmidt et al., 2001;Baldauf et al., 2005). However, the contribution of these inputs to the response properties of PUL neurons is unknown. The cells of the PUL have large visual receptive fields that often lack clear boundaries; they respond more robustly to diffuse illumination than to small visual cues (Godfraind et al., 1972;Mason, 1981 by saccadic eye movements. Sudkamp and Schmidt (2000) identified three general classes of neurons in the feline PUL: "S" neurons are active during saccadic eye movements, "V" neurons are responsive to visual stimuli and unresponsive to eye movements, and "SV" neurons respond to both stationary ON and OFF stimuli and to sudden stimulus shifts.These response properties are similar in many respects to those of neurons in the parietal cortex, an area that establishes extensive reciprocal connections with the PUL (de V Clüver and Campos-Ortega, 1969;Heath and Jones, 1971;Robertson and Cunningham, 1981;Niimi et al., 1983;Raczkowski and Rosenquist, 1983;Avendaño et al., 1985;Olson and Lawler, 1987). In the cat, these cortical areas are primarily located within the middle suprasylvian gyrus (MSg) or cytoarchitectonically in areas 5 and 7 (Gu...

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

“…Complex type II axon terminals formed discrete foci intermingled within more widespread fields of singletons and type I axon terminals. This labelling pattern was similar to that observed in our previous studies of the projection from area 7 to the pulvinar nucleus (Baldauf et al, 2005). It is also similar to the overlap of type I and type II terminals labelled following injections in area 19 (Guillery et al, 2001), although in this latter study the type II terminals tended to form more focused clusters that overlapped with fewer type I terminals.…”

“…7). Finally, we found no correlation between presynaptic terminal type and postsynaptic profile size, although we were able to find such a correlation in a previous study of area 7 terminals in the pulvinar nucleus (Baldauf et al, 2005). This might reflect differences in terminal types originating from area PMLS and area 7 or differences in cell morphologies in the pulvinar and LP nuclei.…”

Ultrastructural analysis of projections to the pulvinar nucleus of the cat. II: Pretectum

“…The following day, the brains were cut into 50-μm-thick coronal sections using a vibratome. Sections containing FDA were processed as described in the accompanying paper (Baldauf et al, 2005). Sections containing pretectal cells labeled with GFM were stained for calbindin or GAD as described below.…”

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).…”

“…Selected areas were mounted on blocks, ultrathin sections (70-80 nm, silvergray interference color) were cut using a diamond knife, and sections were collected on Formvar-coated nickel slot grids. Selected sections were stained for the presence of gamma amino butyric acid (GABA) using previously reported postembedding immunocytochemical techniques (Patel and Bickford 1997;Kelly et al 2003;Baldauf et al 2005;Huppe-Gourgues et al 2006;). The GABA antibody (Sigma, catalogue # A2052, used at a dilution of 1: 1 000-1 :2000) and was tagged with a goat-anti-rabbit antibody conjugated to 15-nm gold particles (Amersham, Arlington Heights, IL).…”