Tarsier Goggles: a virtual reality tool for experiencing the optics of a dark-adapted primate visual system

Despite his ‘confession,’ Darwin never doubted the evolution of complex eyes, a view that has since received overwhelming support (Lamb et al. 2007; Gregory 2008). At the same time, the eyes and visual systems of animals are wonderfully diverse, a fact that fuels the pages of biology textbooks and fires our natural curiosity. Cronin et al. (2014) put it this way: “We humans are visual creatures. We are also introspective and curious, a combination that makes us all by nature amateur visual ecologists (even if we don’t know it). Because our world is dominated by visual sensations, we naturally wonder how other animals see their particular worlds.” On a philosophical level, we can never know the visual world of another organism (Nagel 1974), but the emergence and spread of immersive technologies enables us to try in the service of constructivist pedagogies (Colburn 2000), as a “way of seeing” fundamental concepts in optics and evolution (Scott et al. 1991).

Tarsiers and their visual world

Tarsiers are small (113–142 g) nocturnal primates (Fig. 1a). They are an enduring source of fascination for having enormous eyes, both in absolute size and in proportion to the size of the animal (Fig. 1b). Polyak (1957) concluded that the eye size relative to body size of tarsiers is unmatched by any living vertebrate. The extreme eye size of tarsiers is most likely related to the absence of a tapetum lucidum, the mirror-like structure that results in ‘eye shine’ (Cartmill 1980).

A tapetum lucidum is prevalent among nocturnal mammals, including nocturnal primates, because it increases photon capture and visual sensitivity under low light levels. The absence of a tapetum lucidum in tarsiers is therefore puzzling, and it is interpreted as evidence of an ancestral shift from nocturnality to diurnality followed by a reversion to nocturnality with a diurnally-adapted, tapetum-free eye (Cartmill 1980; Martin and Ross 2005). Thus, the hyper-enlarged eyes of tarsiers are widely viewed as a compensatory adaptation to improve visual sensitivity at night in the absence of a tapetum lucidum.

To appreciate why enlarged eyes are advantageous at night, we can use the dimensions of tarsier eyes to calculate the corresponding parameters for humans. For example, the eye-to-brain volume ratio of tarsiers (see Fig. 1b) can be scaled to human dimensions (see Appendix for calculations), to produce an eye with a diameter of 13.6 cm, the approximate volume of a grapefruit (Fig. 2a). The biological plausibility of this thought experiment is attested by the eyes of colossal squid (Mesonychoteuthis hamiltoni), which are nearly twice as large (Nilsson et al. 2012). Yet, the optic axes of these hypothetical eyes would never align with the visual axes of human binocular vision, so we merged the eyes to bring the optic and visual axes into alignment (Fig. 2b). In theory, such tarsier-inspired eyewear would enhance the visual sensitivity of human users (Fig. 2c), as the enlarged corneas would capture more photons under low light levels.

Physical eyewear could demonstrate these principles, but virtual “lenses” enable the use of filters and interactive elements, essentially transcending physical limitations to create specialized environments for intentional exploration. Such a VRLE is exciting because it can better convey visual sensitivity at night by simulating the benefits of having high densities of rod photoreceptors—tarsiers have > 300,000/mm², whereas humans have ~ 176,000/mm² (Collins et al. 2005). It can also simulate other aspects of tarsier vision. For example, the visual acuity of Philippine tarsiers is estimated at 8.89 c/deg (Veilleux and Christopher 2009), a minimum resolvable angle that can be simulated for human users (Caves and Johnsen 2017). Another distinguishing trait of tarsiers is red-green colorblindness. This trait varies among species, but each phenotype can be simulated (Melin et al. 2013a, b; Moritz et al. 2017). Lastly, a VRLE can simulate the visual field of tarsiers (186°), which we calculated by summing the visual angle of each eye (156.5°; Fig. 1c) and subtracting the area of binocular overlap (127°; Ross 2000).

Collectively, these traits of the tarsier visual system are predicted to result in superior vision (relative to humans) at night, and they are widely interpreted as adaptations for visual predation—tarsiers are exceptional among primates for being 100% faunivorous (Ross 2004; Moritz et al. 2014, 2017). For humans to appreciate the optical and selective advantages of tarsier eyes for accomplishing this visual challenge (navigation and predation in the dark), we conceived and developed a VRLE in the service of education, science communication, and existential reflection. The result—which we call Tarsier Goggles—can simulate human and tarsier vision under varying ambient lighting conditions.

We developed several virtual environments for users to explore within a classroom setting, each of which allows users to alternate between human and tarsier vision, highlighting corresponding differences in brightness, acuity, and color vision. In VR, users begin in an open space (Fig. 3a, b) where they can choose to receive guidance, including tutorials for interface controls and prompts for user behaviors. The first learning environment, “Matrix,” is a 3D lattice of beams that emphasizes human-tarsier differences in visual acuity and color vision (Fig. 3c, d). The second learning environment, “Labyrinth,” is a dark maze-like space that is practically opaque under human visual conditions but navigable as a tarsier, demonstrating the advantages of tarsier visual sensitivity (Fig. 3e, f). The third learning environment, “Bornean Rainforest,” is modeled on the dipterocarp rainforests of Borneo at night (Fig. 3g, h). In this final setting, users can navigate between trees, applying knowledge from previous environments to discover a new worldview—to both experience the worldview of a tarsier and to appreciate why natural selection favored such large eyes. For orientation purposes, two-dimensional (2D) video capture of the preceding progression is available as Additional file 1; however, we recommend that instructors are present to guide first-time student users.

Tarsier Goggles is available for free online (see Availability of data and materials). It is intended to enrich the classroom when the curriculum turns to optics or evolution, topics that have natural and enduring synergies. With even basic awareness of the relevant scientific principles, students or members of the public can wear a VR headset and reflect on how they currently experience the world and how they might through the eyes of another.

At the time of writing, Tarsier Goggles was built in Unity 2018 with SteamVR for the HTC Vive and Vive Pro headsets. We used the Virtual Reality Toolkit (VRTK), an open source library of scripts for Virtual Reality development, to create some menu options and user “teleportation”. This action enables user navigation through each VR environment; it also simulates the vertical clinging-and-leaping behavior of tarsiers when users explore the Bornean Rainforest. We built all other functionalities such as the splash screens and tutorial. For visual effects, we used and modified Unity’s built-in post-processing stack as well as the Colorblind Effect asset created by Project Wilberforce. Our GameObjects, which include trees, grass, bushes, and other virtual structures, were designed and built in Maya as well as downloaded from the Unity Asset Store.

Our initial assessments of Tarsier Goggles were ad hoc and opportunistic, stemming from five demonstrations across a wide range of settings and ages (Fig. 4). Demos were conducted during two on-campus events at Dartmouth that were open to students, faculty, and their families. In addition, we conducted a demo at a professional meeting of biological anthropologists, a group familiar with tarsier visual adaptations. In one case, we worked with middle school (6th grade) students visiting a nonprofit environmental education, research, and avian rehabilitation center in Vermont. Collectively, this broad mix of users (n ≈ 35) provided important feedback for improvements, many of which were implemented in subsequent iterations. Overall, pilot users experienced the effects that we intended—they integrated optical and biological concepts to enrich their understanding of eye evolution and tarsiers.

They also reflected on their experiences. As one Dartmouth professor of engineering put it, “We all think we are seeing what everyone else sees, but in fact we are all seeing something different. I feel connected to animals in a way I haven’t been before.” Another adult user in the profession of science education and outreach added, “It’s not just speculating. It’s actually having it in front of my eyes.” Notably, some children described brief sensations of disorientation, which is not uncommon in VR. Nausea from prolonged use of VR has been reported (Madary and Metzinger 2016), and it is something that educators should consider when using the technology. Best practices for using VRLEs are still in development.

Formal assessment of Tarsier Goggles occurred at an independent private secondary school in New Hampshire serving ∼ 300 students. We focused on two courses, Anthropology (12th grade; 18 student users) and Inquiry to Science (9th grade; 8 student users). We used a central meeting room equipped with a large monitor, which allowed us to project images and orient students to the physical appearance of tarsiers (Fig. 1a) and the relative size of their eyes (Fig. 1b). We also played a brief, muted video of tarsier foraging behavior, in which it is evident that tarsiers are nocturnal visual predators. In the spirit of constructivism (Colburn 2000), there was no preparatory content related to visual anatomy, optics, or natural selection. Instead, we immersed students in the VRLE immediately, allowing them to experience and construct for themselves the adaptive advantages of having enormous eyes at night. Each user trial was 5 min; however, classmates were able to view the user’s learning environment via the monitor (Fig. 5). This configuration stirred considerable commentary and discussion among other students, enriching the learning experience beyond the individual user.

Colburn (2000) argued that classroom demonstrations are at their best when they challenge student preconceptions, forcing them to account for discrepancies between their expectations and observations. Accordingly, we asked students if they were surprised by the differences in tarsier and human visual systems, and 12 of 18 (67%) respondents answered affirmatively (cf. question 6). We attribute this marginally equivocal result to our use of Fig. 1b as an orientation tool. One student said, “I wasn’t that surprised that their vision was that good. Their eyes are slightly larger than their brain so I would have thought their vision would be better.” Such a response reveals twin outcomes: first, it demonstrates the fulfillment of our learning objective; and second, it raises questions about the sequence of learning materials. For this student, prior exposure to Fig. 1b put Tarsier Goggles into the position of confirming rather than challenging expectations, which diminished its effect. An alternative approach in the spirit of constructivism would be to expose students to the VRLE and then prompt them to predict the proportions depicted in Fig. 1b (and perhaps Fig. 2c, which would require them to converge on the same calculations in the Appendix).

Taken together, we believe that Tarsier Goggles has the potential for widespread application. It is poised to complement middle and secondary school curricula in optics and biology; and it is a form of experiential learning that promotes user reflection. In some cases, reflection is the express goal of a VR simulation; for example, In the Eyes of the Animal (http://iteota.com) is a multisensory artistic exploration and technical achievement. An advantage of Tarsier Goggles is that it is designed to be integrated with educational curricula and is targeted to address specific scientific concepts. It may even extend into a museum settings, where people of all backgrounds could enhance their understanding of optics and natural selection via technology that might be new or generally unavailable to them. Further, this VR experience can be expanded to other senses—some tarsiers enjoy exceptional hearing (Ramsier et al. 2012)—or to other visual systems. For example, we have experimented with incorporating the vision of strigiform owls as an example of convergent evolution with tarsiers (Moritz et al. 2014, 2017). Other applications could include human visual impairments, which could further promote greater empathy.