Peak Density and Distribution of Ganglion Cells in the Retinae of Microchiropteran Bats: Implications for Visual Acuity (Part 2 of 2)

Abstract

Wehave estimated the total number, distribution and peak density of retinal ganglion cells (RGCs) in retinal wholemounts of several species of microchiropteran (echolocating) bats. The estimates are based on counts of Nissl-stained, presumed RGCs. The total number of presumed RGCs varies among the species: from about 4,500 in Rhinolophus rouxi to about 120,000 in Macroderma gigas. In addition, in two species (Nyctophilus gouldi and M. gigas), the estimates are based on counts of positively identified RGCs retrogradely labelled with the enzyme horseradish peroxidase injected into the retinorecipient nuclei. In these two species, the numbers and distributions of retrogradely labelled RGCs and Nissl-stained presumed RGCs are very similar. In all six species studied, the peak-density regions of presumed (or positively identified) RGCs are located in the inferotemporal retinae, and the RGC isodensity lines tend to be horizontally elongated. However, the RGC densities in the high-density regions are only 2–4 times greater than those in the low-density regions in the superior retinae. The somal sizes of RGCs vary from 5 to 16 µm in diameter and are unimodally distributed. There is no indication of the existence of distinct morphological classes of RGCs. The axial lenghts of microchiropteran eyes vary from 1.8 mm in R. rouxi to 7.0 mm in M. gigas. For all species the posterior nodal distance (PND) was assumed to be 0.52 of the axial length of the eye. This assumption is based on the analysis of published data concerning schematic eyes of nocturnal vertebrates. These derived values of the PNDs allowed us to calculate the retinal magnification factors and the number of RGCs per degree of visual angle. From these, the upper limits of visual acuity were derived on the basis of the assumptions of the sampling theorem. The estimated upper limits of visual acuity of the six species of echolocating bats vary from about 0.35 cycles/degree in R. rouxi to about 2 cycles/degree in M. gigas. This range is quite similar to the range of visual acuities in murid rodents.

Comparative retinal histomorphometry and visual acuity of three bat species of the genus Artibeus (Phyllostomidae: Stenodermatinae)

“…The RGCs presented cell bodies of different sizes, which suggests that there are different types of RGCs in the retina of these bats (Fig.2). This differentiation in size and types of RGCs was also evidenced by Oyster et al (1981), Pettigrew et al (1988), Dacheux & Raviola (1994), and Brooks et al (1999). Regarding the estimation of the total number of RGCs, which varied significantly between the three species even belonging to the same genus (Table 1), it may be directly related to the retinal area and eye size (Blackwood et al 2010, Eklöf et al 2014.…”

“…The visual acuity or anatomical spatial resolving power was calculated following the equations of Williams & Coletta (1987) and Pettigrew et al (1988). First of all, the posterior nodal distance (PND) should be determined for each eye of the animals and it was calculated using a method established by Pettigrew et al (1988). They proposed that to estimate the PND the axial length of the eyeballs should be multiplied by (0.52).…”

“…The RMF is the linear distance on the retina that subtends 1° of visual angle. Therefore, the RMF was estimated in micrometers per degree (μm/degree) and it was calculated according to the following formula (Pettigrew et al 1988):…”

“…Bats that have a greater visual acuity tend to be frugivorous, such as flying foxes that present a high visual acuity ranging from 2.2 cycles/degree to 5.5 cycles/degree (Pedler & Tilley 1969, Neuweiler 2000, Heffner et al 2008, Müller et al 2007, Coimbra et al 2017 and some echolocating fruit-eating bats, for instance, the three species of Artibeus studied, A. lituratus (1.92 cycles/degree), A. planirostris (1.77 cycles/degree) and A. obscurus (1.50 cycles/degree), A. jamaicensis (1.1 cycles/degree) (Heffner et al 2001), D. cinerea (1.35 cycles/degree), T. georgianus (1.3 cycles/degree) and P. hastatus (1.2 cycles/degree) (Pettigrew et al 1988). In addition, large carnivorous bats such as M. gigas (1.9 cycles/degree) and M. lyra (1.5 cycles/ degree) show a high visual acuity among the echolocating bats as well (Pettigrew et al 1988). Omnivorous species as P. hastatus (1.2 cycles/degree) (Heffner et al 2007) and P. discolor (1.7 cycles/degree) (Hoffmann et al 2016) also have a high visual acuity.…”