Allometric Scaling of the Tectofugal Pathway in Birds

In cartilaginous fishes (Chondrichthyes; sharks, skates and rays (batoids), and holocephalans), the midbrain or mesencephalon can be divided into two parts, the dorsal tectum mesencephali or optic tectum (analogous to the superior colliculus of mammals) and the ventral tegmentum mesencephali. Very little is known about interspecific variation in the relative size and organization of the components of the mesencephalon in these fishes. This study examined the relative development of the optic tectum and the tegmentum in 75 chondrichthyan species representing 32 families. This study also provided a critical assessment of attempts to quantify the size of the optic tectum in these fishes volumetrically using an idealized half-ellipsoid approach (method E), by comparing this method to measurements of the tectum from coronal cross sections (method S). Using species as independent data points and phylogenetically independent contrasts, relationships between the two midbrain structures and both brain and mesencephalon volume were assessed and the relative volume of each brain area (expressed as phylogenetically corrected residuals) was compared among species with different ecological niches (as defined by primary habitat and lifestyle). The relatively largest tecta and tegmenta were found in pelagic coastal/oceanic and oceanic sharks, benthopelagic reef sharks, and benthopelagic coastal sharks. The smallest tecta were found in all benthic sharks and batoids and the majority of bathyal (deep-sea) species. These results were consistent regardless of which method of estimating tectum volume was used. We found a highly significant correlation between optic tectum volume estimates calculated using method E and method S. Taxon-specific variation in the difference between tectum volumes calculated using the two methods appears to reflect variation in both the shape of the optic tectum relative to an idealized half-ellipsoid and the volume of the ventricular cavity. Because the optic tectum is the principal termination site for retinofugal fibers arising from the retinal ganglion cells, the relative size of this brain region has been associated with an increased reliance on vision in other vertebrate groups, including bony fishes. The neuroecological relationships between the relative size of the optic tectum and primary habitat and lifestyle we present here for cartilaginous fishes mirror those established for bony fishes; we speculate that the relative size of the optic tectum and tegmentum similarly reflects the importance of vision and sensory processing in cartilaginous fishes.

Section: Discussionmentioning

confidence: 99%

Allometric Scaling of the Optic Tectum in Cartilaginous Fishes

Yopak

Lisney

2012

“…Given the differences in the organization of the visual streak between these two species [Bravo and Pettigrew, 1981;Wathey and Pettigrew, 1989] and other owls, it is plausible that differences in retinal topography may be reflected centrally in the organization of the optic tectum [Peterson, 1981]. There is some evidence that tectum volume scales very closely with total brain volume in owls [Iwaniuk et al, 2010b]; for example, data on tectum volume from similarly sized barn owl and burrowing owl brains (with volumes of 6,149 and 5,878 mm -3 , respectively) indicate that the tectum accounts for a very similar proportion of the brain in both species (2.22 and 2.53%, respectively). Insufficient information exists at present to speculate any further but a detailed comparative investigation of the retinorecipient brain areas in owls is under way [Gutiérrez-Ibáñez C, Iwaniuk AN, Lisney TJ and Wylie DR, unpubl.…”

Section: Retinotectal Projectionsmentioning

confidence: 99%

“…Such interordinal comparisons yield useful information on broad evolutionary patterns, but whether the same patterns hold true within orders or families is largely unknown [but see Iwaniuk et al, 2010a;Corfield et al, 2011]. In addition, little is known about interspecific variation in retinal topography in birds compared to other vertebrates, especially fishes and mammals [Collin, 1999[Collin, , 2008Iwaniuk et al, 2010b]. Here, we specifically examine eye shape and retinal topography within a single avian order, the owls (Strigiformes).…”

Section: Introductionmentioning

confidence: 99%

Eye Shape and Retinal Topography in Owls (Aves: Strigiformes)

Lisney¹,

Iwaniuk

Bandet

et al. 2012

Self Cite

The eyes of vertebrates show adaptations to the visual environments in which they evolve. For example, eye shape is associated with activity pattern, while retinal topography is related to the symmetry or ‘openness’ of the habitat of a species. Although these relationships are well documented in many vertebrates including birds, the extent to which they hold true for species within the same avian order is not well understood. Owls (Strigiformes) represent an ideal group for the study of interspecific variation in the avian visual system because they are one of very few avian orders to contain species that vary in both activity pattern and habitat preference. Here, we examined interspecific variation in eye shape and retinal topography in nine species of owl. Eye shape (the ratio of corneal diameter to eye axial length) differed among species, with nocturnal species having relatively larger corneal diameters than diurnal species. All the owl species have an area of high retinal ganglion cell (RGC) density in the temporal retina and a visual streak of increased cell density extending across the central retina from temporal to nasal. However, the organization and degree of elongation of the visual streak varied considerably among species and this variation was quantified using H:V ratios. Species that live in open habitats and/or that are more diurnally active have well-defined, elongated visual streaks and high H:V ratios (3.88–2.33). In contrast, most nocturnal and/or forest-dwelling owls have a poorly defined visual streak, a more radially symmetrical arrangement of RGCs and lower H:V ratios (1.77–1.27). The results of a hierarchical cluster analysis indicate that the apparent interspecific variation is associated with activity pattern and habitat as opposed to the phylogenetic relationships among species. In seven species, the presence of a fovea was confirmed and it is suggested that all strigid owls may possess a fovea, whereas the tytonid barn owl (Tyto alba) does not. A size-frequency analysis of cell soma area indicates that a number of different RGC classes are represented in owls, including a population of large RGCs (cell soma area >150 µm²) that resemble the giant RGCs reported in other vertebrates. In conclusion, eye shape and retinal topography in owls vary among species and this variation is associated with different activity patterns and habitat preferences, thereby supporting similar observations in other vertebrates.

“…For example, several studies suggest that a transition from diurnality to nocturnality results in a reduction of the number of RGCs and a reduction of the tectofugal pathway [Kay and Kirk, 2000;Kirk and Kay, 2004;Hall et al, 2009;Iwaniuk et al, 2010b;Corfield et al, 2011]. Therefore, we would expect that nocturnal owl species have a relative smaller tectofugal pathway than more diurnal species.…”

Section: Introductionmentioning

confidence: 97%

“…In recent years, several studies have shown that different demands on the visual system in birds are correlated with variation in the relative size of visual areas in the brain Wylie, 2006, 2007;Iwaniuk et al, 2008Iwaniuk et al, , 2010bCorfield et al, 2011]. However, despite the compelling evidence that differences in activity patterns among owl species are reflected in the organization of the eyes, there has been no attempt so far to correlate these differences with variation in the relative size of visual regions in the brain.…”

Section: Introductionmentioning

confidence: 99%

Comparative Study of Visual Pathways in Owls (Aves: Strigiformes)

Gutiérrez-Ibáñez

Iwaniuk²,

Lisney³

et al. 2012

Self Cite

Although they are usually regarded as nocturnal, owls exhibit a wide range of activity patterns, from strictly nocturnal, to crepuscular or cathemeral, to diurnal. Several studies have shown that these differences in the activity pattern are reflected in differences in eye morphology and retinal organization. Despite the evidence that differences in activity pattern among owl species are reflected in the peripheral visual system, there has been no attempt to correlate these differences with changes in the visual regions in the brain. In this study, we compare the relative size of nuclei in the main visual pathways in nine species of owl that exhibit a wide range of activity patterns. We found marked differences in the relative size of all visual structures among the species studied, both in the tectofugal and the thalamofugal pathway, as well in other retinorecipient nuclei, including the nucleus lentiformis mesencephali, the nucleus of the basal optic root and the nucleus geniculatus lateralis, pars ventralis. We show that the barn owl (Tyto alba), a species widely used in the study of the integration of visual and auditory processing, has reduced visual pathways compared to strigid owls. Our results also suggest there could be a trade-off between the relative size of visual pathways and auditory pathways, similar to that reported in mammals. Finally, our results show that although there is no relationship between activity pattern and the relative size of either the tectofugal or the thalamofugal pathway, there is a positive correlation between the relative size of both visual pathways and the relative number of cells in the retinal ganglion layer.