Gochman et al. Evo Edu Outreach (2019) 12:9 https://doi.org/10.1186/s12052-019-0101-6 Evolution: Education and Outreach COMMENTARY Open Access Tarsier Goggles: a virtual reality tool for experiencing the optics of a dark-adapted primate visual system Samuel R. Gochman1,2* , Marilyn Morano Lord3, Naman Goyal2, Kristie Chow2, Benjamin K. Cooper2, Lauren K. Gray2, Stephanie X. Guo2, Kylie A. Hill2, Stephen K. Liao2, Shiyao Peng2, Hyun J. Seong2, Alma Wang2, Eun K. Yoon2, Shirley Zhang2, Erica Lobel2, Tim Tregubov2 and Nathaniel J. Dominy1* Abstract Charles Darwin viewed eyes as the epitome of evolution by natural selection, describing them as organs of extreme perfection and complication. The visual system is therefore fertile ground for teaching fundamental concepts in optics and biology, subjects with scant representation during the rise and spread of immersive technologies in K-12 educa- tion. The visual system is an ideal topic for three-dimensional (3D) virtual reality learning environments (VRLEs), and here we describe a 3D VRLE that simulates the vision of a tarsier, a nocturnal primate that lives in southeast Asia. Tarsi- ers are an enduring source of fascination for having enormous eyes, both in absolute size and in proportion to the size of the animal. Our motivation for developing a tarsier-inspired VRLE, or Tarsier Goggles, is to demonstrate the optical and selective advantages of hyperenlarged eyes for nocturnal visual predation. In addition to greater visual sensitiv- ity, users also experience reductions in visual acuity and color vision. On a philosophical level, we can never know the visual world of another organism, but advances in 3D VRLEs allow us to try in the service of experiential learning and educational outreach. Keywords: Constructivist learning theory, Tarsius bancanus, Tarsier, Virtual reality, Optics, Natural selection, Vision Background Despite his ‘confession,’ Darwin never doubted the evo- Te eye is an exquisite anatomical structure and fer- lution of complex eyes, a view that has since received tile ground for demonstrating core concepts in phys- overwhelming support (Lamb et al. 2007; Gregory 2008). ics (optics) and biology (evolution by natural selection), At the same time, the eyes and visual systems of animals a pattern that began with Darwin himself. He described are wonderfully diverse, a fact that fuels the pages of biol- eyes as “organ[s] of extreme perfection and complication” ogy textbooks and fres our natural curiosity. Cronin et al. (Darwin 1859, p. 186) and he used them as foil for oppo- (2014) put it this way: “We humans are visual creatures. sition in one of his most-quoted sentences: We are also introspective and curious, a combination that makes us all by nature amateur visual ecologists (even To suppose that the eye with all its inimitable con- if we don’t know it). Because our world is dominated by trivances for adjusting the focus to diferent dis- visual sensations, we naturally wonder how other animals tances, for admitting diferent amounts of light, and see their particular worlds.” On a philosophical level, we for the correction of spherical and chromatic aber- can never know the visual world of another organism ration, could have been formed by natural selection, (Nagel 1974), but the emergence and spread of immersive seems, I freely confess, absurd in the highest degree. technologies enables us to try in the service of construc- *Correspondence: [email protected]; tivist pedagogies (Colburn 2000), as a “way of seeing” [email protected] fundamental concepts in optics and evolution (Scott et al. 1 Departments of Anthropology and Biological Sciences, Dartmouth College, Hanover, NH 03755, USA 1991). Full list of author information is available at the end of the article © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/ publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Gochman et al. Evo Edu Outreach (2019) 12:9 Page 2 of 8 3D virtual reality learning environments (VRLEs) Tree-dimensional (3D) virtual reality learning environ- ments (VRLEs) are well suited to constructivism, espe- cially when students must form 3D representations of course material or interact with a learning environment to construct knowledge (reviews: Huang et al. 2010; Merchant et al. 2014). Accordingly, the development and deployment of 3D VRLEs has expanded rapidly in K-12 and higher education, especially medical education (Wu et al. 2013; Jang et al. 2017); indeed, the anatomi- cal education of medical students is a major catalyst for 3D VRLE technology. Te practical value of 3D VRLEs for learning human anatomy hints at wider applications within K-12 biological education. For example, the prin- ciples of natural selection and evolution is another topic that invites constructivist pedagogies (Kalinowski et al. Fig. 1 a Bornean tarsier (Tarsius bancanus) under nocturnal 2013; Lee et al. 2017; Prins et al. 2017). Here we describe conditions; note the extreme dilation of the pupil (photograph by David Haring, reproduced with permission). b Anatomical preparation a 3D VRLE with this goal in mind. It is intended to dem- of the eye and brain of T. bancanus (modifed from Sprankel 1965), onstrate the principles of visual optics and natural selec- illustrating the comparable volume of the two structures (Castenholz tion in a way that constructs knowledge and stimulates 1984). The eyes of T. bancanus are therefore enormous, both in user refection on diverse worldviews. Te inspiration absolute size and in proportion to the size of the animal. c Geometry for our 3D VRLE is the tarsier, a primate with an extreme of the tarsier eye (modifed from Castenholz 1984) illustrating our calculation of the visual angle visual system. Tarsiers and their visual world Tarsiers are small (113–142 g) nocturnal primates is attested by the eyes of colossal squid (Mesonychoteu- (Fig. 1a). Tey are an enduring source of fascination for this hamiltoni), which are nearly twice as large (Nilsson having enormous eyes, both in absolute size and in pro- et al. 2012). Yet, the optic axes of these hypothetical eyes portion to the size of the animal (Fig. 1b). Polyak (1957) would never align with the visual axes of human bin- concluded that the eye size relative to body size of tar- ocular vision, so we merged the eyes to bring the optic siers is unmatched by any living vertebrate. Te extreme and visual axes into alignment (Fig. 2b). In theory, such eye size of tarsiers is most likely related to the absence of tarsier-inspired eyewear would enhance the visual sen- a tapetum lucidum, the mirror-like structure that results sitivity of human users (Fig. 2c), as the enlarged corneas in ‘eye shine’ (Cartmill 1980). would capture more photons under low light levels. A tapetum lucidum is prevalent among nocturnal Physical eyewear could demonstrate these principles, mammals, including nocturnal primates, because it but virtual “lenses” enable the use of flters and interac- increases photon capture and visual sensitivity under low tive elements, essentially transcending physical limita- light levels. Te absence of a tapetum lucidum in tarsiers tions to create specialized environments for intentional is therefore puzzling, and it is interpreted as evidence of exploration. Such a VRLE is exciting because it can bet- an ancestral shift from nocturnality to diurnality followed ter convey visual sensitivity at night by simulating the by a reversion to nocturnality with a diurnally-adapted, benefts of having high densities of rod photorecep- 2 tapetum-free eye (Cartmill 1980; Martin and Ross 2005). tors—tarsiers have > 300,000/mm , whereas humans 2 Tus, the hyper-enlarged eyes of tarsiers are widely have ~ 176,000/mm (Collins et al. 2005). It can also sim- viewed as a compensatory adaptation to improve visual ulate other aspects of tarsier vision. For example, the vis- sensitivity at night in the absence of a tapetum lucidum. ual acuity of Philippine tarsiers is estimated at 8.89 c/deg To appreciate why enlarged eyes are advantageous at (Veilleux and Christopher 2009), a minimum resolvable night, we can use the dimensions of tarsier eyes to cal- angle that can be simulated for human users (Caves and culate the corresponding parameters for humans. For Johnsen 2017). Another distinguishing trait of tarsiers is example, the eye-to-brain volume ratio of tarsiers (see red-green colorblindness. Tis trait varies among spe- Fig. 1b) can be scaled to human dimensions (see Appen- cies, but each phenotype can be simulated (Melin et al. dix for calculations), to produce an eye with a diameter of 2013a, b; Moritz et al. 2017). Lastly, a VRLE can simu- 13.6 cm, the approximate volume of a grapefruit (Fig. 2a). late the visual feld of tarsiers (186°), which we calculated Te biological plausibility of this thought experiment by summing the visual angle of each eye (156.5°; Fig. 1c) Gochman et al. Evo Edu Outreach (2019) 12:9 Page 3 of 8 Fig. 2 a Hypothetical size of tarsier eyes when scaled to human dimensions. We used the mean interpupillary distance reported for humans (6.3 cm) to merge the eyes and align the optic and visual axes. b Scaling of the hypothetical eyes in relation to a human head. c Rendering to simulate the scaled eyes on a human user and subtracting the area of binocular overlap (127°; Ross vision, highlighting corresponding diferences in bright- 2000).