Synaptic organization of striate cortex projections in the tree shrew: A comparison of the claustrum and dorsal thalamus

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The claustrum is an enigmatic structure of the telencephalon, interposed between the cerebral cortex and basal ganglia. Perhaps the most intriguing feature of the claustrum is that it is reciprocally connected with most areas of the cortex (for review see Goll et al., 2015). These vast connections have prompted speculation and study of the potential role of the claustrum in a variety of processes, including multisensory integration, attention allocation, novelty detection, and consciousness (see, e.g., Edelstein and Denaro, 2004; Crick and Koch, 2005; Smythies et al., 2012; Remedios et al., 2014). However, relatively little information is available regarding the specific functions of either claustrocortical or corticoclaustral connections.
The claustrum is a particularly well‐developed structure in the tree shrew (Tupaia belangeri), a species that is considered to represent a prototype of early prosimian primates. Although now classified in the order Scadentia, the brains of tree shrews display many primate‐like features, particularly within visual structures (Holdefer and Norton, 1995; Fitzpatrick, 1996). In fact, reflecting the importance of vision for tree shrew behavior, cortical and subcortical visual structures make up a large proportion of the tree shrew brain. This elaboration of visual pathways is further demonstrated by the substantial reciprocal connections between the striate cortex and the claustrum found in this species (Carey et al., 1979, 1980; Carey and Neal, 1986).
In addition to the claustrum, the striate cortex of the tree shrew is reciprocally connected with two other subcortical structures, the dorsal lateral geniculate nucleus (dLGN) and the ventral pulvinar nucleus (Pv; Carey et al., 1979; Usrey et al., 1992; Usrey and Fitzpatrick, 1996; Lyon et al., 2003). The striate cortex projections to these two thalamic nuclei arise from distinct cell types (Usrey and Fitzpatrick, 1996), and it has been proposed that these corticothalamic projections carry out distinct functions. Because dLGN activity is driven primarily by direct input from the retina, corticogeniculate projections are considered to be “feedback” projections that do not dramatically alter receptive field properties but instead modulate the responsiveness of dLGN neurons (Sherman and Guillery, 1998; Briggs and Usrey, 2008). In contrast, within the pulvinar nucleus, a population of corticopulvinar terminals has been found to be structurally and physiologically similar to retinogeniculate terminals (Guillery et al., 2001; Li et al., 2003a; Huppé‐Gourgues et al., 2006). Therefore, input from the striate cortex is thought to drive the receptive field properties of pulvinar neurons, and the striate‐recipient zone of the pulvinar nucleus is recognized as a “higher order” thalamic nucleus to reflect this strong link to cortical rather than subcortical activity patterns (Sherman and Guillery, 1998).
The purpose of this study was to compare directly the synaptic organization of projections from the striate cortex to the claustrum, dLGN, and Pv of the same species to identify similarities or differences in these projections that might reveal clues to the function of the claustrum. In other words, we seek to determine whether corticoclaustral projections display ultrastructural features that may be associated with “driving” (large terminals that innervate proximal dendrites) or “modulating” (smaller terminals that innervate more distal dendrites) inputs (for review see Bickford, 2016). We additionally stained tissue sections to reveal the presence of γ‐aminobutyric acid (GABA). This allowed us to identify non‐GABAergic projection cells and GABAergic interneurons within each structure and to determine the degree to which each of these cell types receives input from the striate cortex. Our results indicate that, although some similarities between claustrum and thalamic circuits can be identified, the synaptic organization of the claustrum does not suggest a driver/modulator framework. Instead, the circuitry of the claustrum suggests an integration of convergent cortical inputs, gated by GABAergic circuits.
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