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

Abstract

The lateral posterior (LP) nucleus is a higher order thalamic nucleus that is believed to play a key role in the transmission of visual information between cortical areas. Two types of cortical terminals have been identified in higher order nuclei, large (type II) and smaller (type I), which have been proposed to drive and modulate, respectively, the response properties of thalamic cells (Sherman and Guillery [1998] Proc. Natl. Acad. Sci. U. S. A. 95:7121-7126). The aim of this study was to assess and compare the relative contribution of driver and modulator inputs to the LP nucleus that originate from the posteromedial part of the lateral suprasylvian cortex (PMLS) and area 17. To achieve this goal, the anterograde tracers biotinylated dextran amine (BDA) or Phaseolus vulgaris leucoagglutinin (PHAL) were injected into area 17 or PMLS. Results indicate that area 17 injections preferentially labelled large terminals, whereas PMLS injections preferentially labelled small terminals. A detailed analysis of PMLS terminal morphology revealed at least four categories of terminals: small type I terminals (57%), medium-sized to large singletons (30%), large terminals in arrangements of intermediate complexity (8%), and large terminals that form arrangements resembling rosettes (5%). Ultrastructural analysis and postembedding immunocytochemical staining for γ-aminobutyric acid (GABA) distinguished two types of labelled PMLS terminals: small profiles with round vesicles (RS profiles) that contacted mostly non-GABAergic dendrites outside of glomeruli and large profiles with round vesicles (RL profiles) that contacted non-GABAergic dendrites (55%) and GABAergic dendritic terminals (45%) in glomeruli. RL profiles likely include singleton, intermediate, and rosette terminals, although future studies are needed to establish definitively the relationship between light microscopic morphology and ultrastructural features. All terminals types appeared to be involved in reciprocal corticothalamocortical connections as a result of an intermingling of terminals labelled by anterograde transport and cells labelled by retrograde transport. In conclusion, our results indicate that the origin of the driver inputs reaching the LP nucleus is not restricted to the primary visual cortex and that extrastriate visual areas might also contribute to the basic organization of visual receptive fields of neurons in this higher order nucleus. *Correspondence to: Christian Casanova, Laboratoire des Neurosciences de la Vision, École d'Optométrie, Université de Montréal, C.P. 6128 Succ. Centre-Ville, Montréal, Québec, Canada H3C 3J7. E-mail: christian.casanova@umontreal.ca. D. Boire's current address is Département de Chimie-Biologie, Université du Québec à Trois-Rivières, Trois-Rivières, Québec, Canada. The cat lateral posterior (LP) and pulvinar nuclei receive input from a wide array of cortical areas concerned with vision or visuomotor control. These areas include cortical areas 17, 18, 19, 20, and 21 as well as the variety of visual areas t...

Two Streams of Attention-Dependent β Activity in the Striate Recipient Zone of Cat's Lateral Posterior–Pulvinar Complex

“…The two functionally distinct regions of LPl-c may thus represent integrative relays for separate corticothalamocortical streams of information processing, dealing with different aspects of visual stimuli. This proposal is strongly supported by previous studies of anatomical connections (Berson and Graybiel, 1978;Updyke, 1983;Abramson and Chalupa, 1988;Kelly et al, 2003;Huppe-Gourgues et al, 2006) and single cell recordings from anesthetized cats (Casanova et al, 1989;Chalupa and Abramson, 1989;Dumbrava et al, 2001). The hypothesis proposed here is based on our clear-cut statistical analysis which matched two different bands of increased ␤ attentional activity with anatomically distinct locations at three levels of visual information processing (primary cortices, LPl-c and MSS) and additionally confirmed by correlation data in the functioning network.…”

“…6). Although the number of our recording sites in LP1-c is limited (10 in 11 cats), the proposed division perfectly matches the diverse morphology and connectivity of these subregions (Berson and Graybiel, 1978;Updyke, 1983;Abramson and Chalupa, 1988;Garey et al, 1991;Kelly et al, 2003;Huppe-Gourgues et al, 2006) and differences of their neuronal responses in anesthetized cats (Casanova et al, 1989;Chalupa and Abramson, 1989;Hutchins and Updyke, 1989;Dumbrava et al, 2001). There is, however, a discrepancy between our data and those of others with regard to the extent of the dorsolateral region bordering on the pulvinar.…”

“…The available data suggests a causative link between ␤ activity and the known anatomical connections of MSS (Garey et al, 1991;Huppe-Gourgues et al, 2006), which could link ␤ activity between the primary visual cortex and MSS.…”

“…Among the latter, the middle suprasylvian region was chosen because of its strong interconnections with the LP-P (Garey et al, 1991;Payne and Lomber, 2003;Huppe-Gourgues et al, 2006) and its involvement in visually guided behavior (Kiefer et al, 1989;Shupert et al, 1993;Rudolph and Pasternak, 1996;Ouellette et al, 2004). The phasecorrelation analysis between the recorded signals was used to determine the dynamics of functional connections within the network during attentive behavior.…”

Signal processing in the tectothalamic pathway.

“…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).…”