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

Abstract

The tree shrew (Tupaia belangeri) striate cortex is reciprocally connected with the dorsal lateral geniculate nucleus (dLGN), the ventral pulvinar nucleus (Pv), and the claustrum. In the Pv and dLGN, striate cortex projections are thought to either strongly “drive”, or more subtly “modulate” activity patterns respectively. To provide clues to the function of the claustrum, we compared the synaptic arrangements of striate cortex projections to the dLGN, Pv and claustrum using anterograde tracing and electron microscopy. Tissue was additionally stained with antibodies against gamma amino butyric acid (GABA) to identify GABAergic interneurons and nonGABAergic projection cells. The size of striate cortex terminals was largest in the Pv (0.94 ± 0.08 μm2), intermediate in the claustrum (0.34 ± 0.02 μm2) and smallest in the dLGN (0.24 ± 0.01 μm2). Contacts on interneurons were most common in the Pv (39%), intermediate in the claustrum (15%) and least common in the dLGN (12%). In the claustrum, nonGABAergic terminals (0.34 ± 0.01 μm2) and striate cortex terminals were not significantly different in size. The largest terminals in the claustrum were GABAergic (0.51 ± 0.02 μm2) and these terminals contacted dendrites and somata that were significantly larger (1.90 ± 0.30 μm2) than those contacted by cortex or nonGABAergic terminals (0.28 ± 0.02 μm2 and 0.25 ± 0.02 μm2 respectively). Our results indicate that the synaptic organization of the claustrum does not correspond with a driver/modulator framework. Instead, the circuitry of the claustrum suggests an integration of convergent cortical inputs, gated by GABAergic circuits.

The mouse pulvinar nucleus: Organization of the tectorecipient zones

“…The terminals that arise from layer V cells are significantly larger than corticogeniculate terminals or tectopulvinar terminals (rat; Bourassa and Deschênes, 1995; tree shrew; Chomsung et al, 2008; Day-Brown et al, 2016; cat; Guillery et al, 2001; Huppé-Gourgues et al, 2006; Kelly et al, 2003; rat; Li et al, 2003c; Masterson et al, 2009), and similar large V1 corticopulvinar terminals are found in the mouse (Figure 5A, 7A). …”

The relationship between the claustrum and endopiriform nucleus: A perspective towards consensus on cross‐species homology

“…boutons that extend off the axon (da Costa et al, 2010;Smith et al, 2017), which is consistent with "modulator" type synapses that exhibit paired-pulse facilitation on their postsynaptic targets (Sherman & Guillery, 1998). However, there is some controversy surrounding the "driver/modulator" categorization for claustral synapses, especially for corticoclaustral synapses Day-Brown et al, 2017).…”

“…As shown in the photomicrograph in Figure d, these terminals appear as small (<0.5 μm diameter), “mushroom‐like” boutons that extend off the axon (da Costa et al, ; Smith et al, ), which is consistent with “modulator” type synapses that exhibit paired‐pulse facilitation on their postsynaptic targets (Sherman & Guillery, ). However, there is some controversy surrounding the “driver/modulator” categorization for claustral synapses, especially for corticoclaustral synapses (Brown et al, ; Day‐Brown et al, ). Specifically, these authors measured the size of corticoclaustral synapses (0.34 ± 0.02 μm 2 ) and compared them to the size of corticothalamic modulators (0.24 ± 0.01 μm 2 ) and corticothalamic drivers (0.94 ± 0.08 μm 2 ).…”

Signal processing in the tectothalamic pathway.

“…In tree shrews, projections from the striate cortex to the extrageniculate thalamus are limited to the ventral pulvinar nucleus and lateral intermediate nucleus (Huerta et al 1985;Day-Brown et al 2007), and, as demonstrated in the current study, only the temporal cortex projects to the Pd and Pc. In contrast, the tectorecipient zones of the primate pulvinar nucleus receive extensive input from both the striate and temporal cortex (Glendenning et al 1975;Symonds and Kaas 1978;Lin and Kaas 1979;Diamond 1980, 1981;Wall et al 1982;Ungerleider et al 1983).…”