The architecture of claustrum and related limbic cortical regions in Carollia perspicillata revealed by latexin and calcium-binding proteins

Abstract

Claustrum is a region of grey matter between striatum and cerebral cortex that is among the most well-connected structures in the brain. It is hypothesized to function as a high-level coordinator of brain-wide activities like sensory integration, attention, sleep, and consciousness. The exact anatomical boundaries of claustrum have been controversial, and claustral subregions have not been well-defined. This may be in part due to its compact structure in rodents and other commonly studied species. In contrast, Seba’s short-tailed fruit (Carollia perspicillata) bat has a remarkably large claustrum, lending itself as a model and magnified view for investigating claustrum. We studied the distributions of the claustral marker latexin and the calcium-binding proteins calbindin, calretinin, and parvalbumin in claustrum. Using these markers, we defined clear claustral boundaries and several distinct subregions. The calcium-binding proteins, which mark different subtypes of inhibitory neurons, were differentially distributed among subregions, suggesting that these regions are under the control of different inhibitory systems. In addition to having a large claustrum, Carollia is a relatively long-lived species, lending itself as a model for the neurobiology of aging and neurodegeneration. Two brain regions highly affected in the aging process are retrosplenial cortex (Brodmann areas 29 and 30) and hippocampus. In the course of this work, we found latexin was present in retrosplenial cortex, a region involved in memory and navigation, but only in Brodmann areas 29a and 29b. This distinct division of retrosplenial cortex differs from cytoarchitecturally-defined divisions but aligns with connectivity evidence that supports grouping areas 29a and 29b separate from areas 29c and 30. Finally, we found, several features of Carollia hippocampus, including a compacted CA3 cell layer and a prosubiculum, that are also present in primate but not rodent hippocampus. Due to these unique neuroanatomical features, Carollia may offer advantages in studying claustrum and other limbic cortical structures, especially in the context of aging, that are not present in more commonly studied model species.