The visual system in subterranean African mole-rats (Rodentia, Bathyergidae): Retina, subcortical visual nuclei and primary visual cortex

doi:10.1016/j.brainresbull.2007.10.055

Brain Research Bulletin

Volume 75, Issues 2–4, 18 March 2008, Pages 356-364

https://doi.org/10.1016/j.brainresbull.2007.10.055 Get rights and content

Abstract

We have studied the visual system of subterranean mole-rats of the rodent family Bathyergidae, for which light and vision seem of little importance. The eye diameter varies between 3.5 mm in Bathyergus suillus and 1.3 mm in Heterocephalus glaber. The small superficial eyes have features typical of sighted animals (clear optics, well-developed pupil and well-organized retina) and appear suited for proper image formation. The retinae are rod-dominated but possess rather high cone proportions of about 10%. The total number of retinal ganglion cells and optic nerve fibres ranges between 6000 in Bathyergus suillus and 2100 in Heliophobius argenteocinereus. Visual acuity (estimated from counts of peak ganglion cell density and axial length of the eye) is low, ranging between 0.3 and 0.5 cycles/degree. The retina projects to all the visual structures described in surface-dwelling sighted rodents. The suprachiasmatic nucleus is large and receives bilateral retinal input. All other visual nuclei are reduced in size and receive almost exclusively contralateral retinal projections of varying magnitude. The primary visual cortex is small and, in comparison to other rodents, displaced laterally. In conclusion, the African mole-rats possess relatively well-developed functional visual subsystems involved in photoperiodicity, form and brightness discrimination. In contrast, visual subsystems involved in coordination of visuomotor reflexes are severely reduced. This pattern suggests the retention of basic visual capabilities. Residual vision may enable subterranean mammals to localize breaches in the burrows that let in light thus providing a cue to enable mole-rats to reseal such entry points and to prevent entry of predators.

Introduction

Until recently, our understanding of the visual system of subterranean mammals was mainly based on seminal studies in the blind mole-rat Spalax ehrenbergi which has regressed and rudimentary visual structures [2], [4], [22]. Over the last years, studies covering a larger range of subterranean mammalian species have ‘unearthed’ an unexpected diversity of ocular and retinal features [21], [28]. Similarly, it was shown that not all visual brain nuclei are equally degenerate across species [reviewed in 21]. Taken together, these findings suggest different visual capabilities and adaptations in different subterranean rodents. They challenge the widely held view that vision is an expendable sense underground. Here we describe the visual system of the African mole-rats (Bathyergidae), a group of rodents unrelated to Spalax, which have independently adopted a strictly subterranean mode of life, and discuss the potential role of vision for these “blind” creatures.

Section snippets

Eye morphology

Eye sizes vary substantially across bathyergid species (Fig. 1). The axial length of the eye ranges between 3.5 mm in Bathyergus suillus and 1.3 mm in Heterocephalus glaber. In contrast to the blind mole-rat, African mole-rat eyes feature normal properties: eyelids, clear optics, an iris with a pupillary aperture, and a well-developed retina lining the back of the eye (Fig. 1). This indicates the capability of image-forming vision.

Small eye size limits the image size on the retina, resulting in

Retina

The general morphology and layering of the retina is preserved, but the thickness of the layers varies greatly across species, indicating different processing capacities (Fig. 2).

Subcortical visual system

To date, retinal projections have been studied in the bathyergids Cryptomys pretoriae [18], Fukomys anselli [20] and Heterocephalus glaber [5]. Quantitative data on the relative distribution and the density of the retinal projections are only available for F. anselli (Fig. 3B, C). All subcortical visual centres except for the suprachiasmatic nucleus (SCN) are cytoarchitecturally poorly developed and reduced in size, while the degree of reduction differs between nuclei. The lateral geniculate

Visual cortex

A search for the primary visual cortex has been conducted in three bathyergid species, but the available evidence remains controversial. Electrophysiological mapping experiments provided no evidence for the existence of visually responsive cortical areas in Heterocephalus glaber [1], [11]. In contrast, our anatomical study utilizing retrograde tracing and the technique of flattening and sectioning the cortex to visualize area boundaries has evidenced the presence of a primary visual cortex in

Oculomotor nuclei

A surprisingly well-developed oculomotor nucleus was described in Fukomys anselli [20], and cholinergic oculomotor and trochlear nuclei were described in Cryptomys pretoriae [6]. The trochlear nucleus is reported to be composed of very few motoneurons and partly merged with the posterior portion of the oculomotor nucleus. It is likely that most of the oculomotor nucleus motoneurons innervate the well-developed musculus retractor bulbi, which may serve the protective retraction of the eye during

Role of vision

Anecdotal observations suggest that bathyergids are oblivious to light stimuli such as moving objects or full-field light flashes [7], [24], [12]. This is in line with severe reduction of the midbrain structures subserving coordination of visuomotor reflexes (NOT, SC, AOS) and indicates that bathyergids are poorly equipped for orientation in the three-dimensional visual environment that is encountered by a rodent active on the surface. The absence of spatially appropriate orientation responses

Acknowledgments

We thank Walter Hofer and Jitka Koláčková-Sedláčková for excellent histological assistance; Jennifer U.M. Jarvis, M. Justin O’Riain and Radim Šumera for providing Bathyergus suillus, Heterocephalus glaber and Heliophobius argenteocinereus, respectively; and Jan Burda for drawing Fig. 4D. Our work was supported by grants from the DFG (BU 717/10-3; to HB), the Czech Science Foundation (206/06/1469; to PN), the Ministry of Education, Youth and Sport of the Czech Republic (0021620828; to PN),

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ReviewThe visual system in subterranean African mole-rats (Rodentia, Bathyergidae): Retina, subcortical visual nuclei and primary visual cortex

Abstract

Introduction

Section snippets

Eye morphology

Retina

Subcortical visual system

Visual cortex

Oculomotor nuclei

Role of vision

Acknowledgments

J. Chem. Neuroanat.

Physiol. Behav.

Brain. Res. Rev.

Physiol. Behav.

Brain Res.

Brain Res. Bull.

Neuroscience

Neuroscience

Physiol. Behav.

Physiol. Behav.

Dev. Brain Res.

Physiol. Behav.

Physiol. Behav.

Anim. Behav.

Brain Res.

Somatosensory cortex dominated by the representation of teeth in the naked mole-rat brain

Proc. Natl. Acad. Sci. U.S.A.

The retina of Spalax ehrenbergi: novel histologic features supportive of a modified photosensory role

Invest. Ophthalmol. Vis. Sci.

The eye of the African mole-rat Cryptomys anselli: to see or not to see?

Eur. J. Neurosci.

Visual system of a naturally microphthalmic mammal: the blind mole rat, Spalax ehrenbergi

J. Comp. Neurol.

Central visual system of the naked mole-rat (Heterocephalus glaber)

Anat. Rec. A

Review
The visual system in subterranean African mole-rats (Rodentia, Bathyergidae): Retina, subcortical visual nuclei and primary visual cortex