Does the visual system of the flying fox resemble that of primates? The distribution of calcium-binding proteins in the primary visual pathway ofPteropus poliocephalus

Abstract

It has been proposed that flying foxes and echolocating bats evolved independently from early mammalian ancestors in such a way that flying foxes form one of the suborders most closely related to primates. A major piece of evidence offered in support of a flying fox-primate link is the highly developed visual system of flying foxes, which is theorized to be primate-like in several different ways. Because the calcium-binding proteins parvalbumin (PV) and calbindin (CB) show distinct and consistent distributions in the primate visual system, the distribution of these same proteins was examined in the flying fox (Pteropus poliocephalus) visual system. Standard immunocytochemical techniques reveal that PV labeling within the lateral geniculate nucleus (LGN) of the flying fox is sparse, with clearly labeled cells located only within layer 1, adjacent to the optic tract. CB labeling in the LGN is profuse, with cells labeled in all layers throughout the nucleus. Double labeling reveals that all PVϩ cells also contain CB, and that these cells are among the largest in the LGN. In primary visual cortex (V1) PV and CB label different classes of nonpyramidal neurons. PVϩ cells are found in all cortical layers, although labeled cells are found only rarely in layer I. CBϩ cells are found primarily in layers II and III. The density of PVϩ neuropil correlates with the density of cytochrome oxidase staining; however, no COϩ or PVϩ or CBϩ patches or blobs are found in V1. These results show that the distribution of calcium-binding proteins in the flying fox LGN is unlike that found in primates, in which antibodies for PV and CB label specific separate populations of relay cells that exist in different layers. Indeed, the pattern of calcium-binding protein distribution in the flying fox LGN is different from that reported in any other terrestrial mammal. Within V1 no PVϩ patches, CO blobs, or patchy distribution of CBϩ neuropil that might reveal interblobs characteristic of primate V1 are found; however, PV and CB are found in separate populations of non-pyramidal neurons. The types of V1 cells labeled with antibodies to PV and CB in all mammals examined including the flying fox suggest that the similarities in the cellular distribution of these proteins in cortex reflect the fact that this feature is common to all mammals.

Neocortical neuron types in Xenarthra and Afrotheria: implications for brain evolution in mammals

“…The morphological classes of interneurons defined by their expression of calcium-binding proteins and NPY in our study of atlantogenatans closely resembled the major types that have been described extensively in other eutherian mammals Ferrer 1994, 1995;Clemo et al 2003;Desgent et al 2005;Gao et al 2000;Glezer et al 1992Glezer et al , 1993Glezer et al , 1998Gonchar and Burkhalter 1997;Hof et al 1996aHof et al , 1999Hogan and Berman 1994;Ichida et al 2000;Lund and Lewis 1993;Nimchinsky et al 1997;Park et al 2000;Van Brederode et al 1990, as well as marsupials , and the monotreme echidna (Hassiotis et al 2005). This suggests that the common ancestor of all mammals possessed many of the same interneuron types expressing similar neurochemical profiles and that these cell classes were retained in all descendants.…”

Retinofugal Projections Into Visual Brain Structures in the Bat Artibeus planirostris: A CTb Study

“…Larger (mean area = 149.1 μm 2 ) cells were observed in the dLGN compared to those in the SC and PNT of A. planirostris . A previous study in the gray-headed flying fox ( Pteropus poliocephalus ) revealed small neurons (106 μm 2 ) in the dLGN (Ichida et al, 2000 ) compared to those in the dLGN in A. planirostris . Scalia et al ( 2015 ) have performed an extensive study of subcortical visual centers in the bat Carolia perspicilata .…”

“…Previous studies in bat, using fiber degeneration after eye removal or an intraocular CTb injection have shown lateral and medial layers in the dLGN, even though no quantitative approach has been performed (Cotter and Pierson Pentney, 1979 ; Cotter, 1985 ; Covey et al, 1987 ). In addition, three layers were identified in Pteropus poliocephalus (Ichida et al, 2000 ; Manger and Rosa, 2005 ) and six layers are classically described in primates (Fitzpatrick et al, 1980 ; Callaway, 2005 ). Taken together, these findings suggest that the visual system in bats, including A. planrostris , might function as a series of parallel pathways, conveying different aspects of the visual information, similar to that seen in upper vertebrates, which to a great extent orient their behavior by sight.…”

“…Additionally, a laminar segregation of the retinal fibers in the dLGN is relatively clear in pteropodid bats (Cotter, 1981 ; formerly classified as Megachiropterans). This laminar segregation is present in species that are heavily reliant on visual cues for their normal behavior, such as carnivores, primates, tree shrews and flying foxes (e.g., Kaas et al, 1978 ; Dreher, 1986 ; Casagrande and Norton, 1991 ; Garey et al, 1991 ; Rosa et al, 1996 ; Ichida et al, 2000 ; Lyon et al, 2003 ; for reviews).…”

Ionotropic Glutamate Receptor GluR1 in the Visual Cortex of Hamster: Distribution and Co-Localization with Calcium-Binding Proteins and GABA

“…GluR1-immunoreactive (IR) neurons in the visual cortex of the monkey [3] and rat [15] have been described. Calcium-binding proteins are localized in the visual cortex of several mammalsvincluding human [2, 11, 20, 33–36], monkey [2, 8, 12, 14, 19, 20, 40, 59, 60], dolphin [11, 12], cat [9, 21, 24, 54], rabbit [45], flying fox [23], ferret [10], rat [5, 13, 37], mouse [46], and hamster [31]. …”