Journal of Comparative Physiology A

, Volume 191, Issue 2, pp 125–134 | Cite as

Photoreceptors and photopigments in a subterranean rodent, the pocket gopher (Thomomys bottae)

  • Gary A. Williams
  • Jack B. Calderone
  • Gerald H. JacobsEmail author
Original Paper


Pocket gophers (Thomomys bottae) are rodents that spend much of their lives in near-lightless subterranean burrows. The visual adaptations associated with this extreme environment were investigated by making anatomical observations of retinal organization and by recording retinal responses to photic stimulation. The size of the eye is within the normal range for rodents, the lens transmits light well down into the ultraviolet, and the retina conforms to the normal mammalian plan. Electroretinogram recording revealed the presence of three types of photopigments, a rod pigment with a spectral peak of about 495 nm and two types of cone pigment with respective peak values of about 367 nm (UV) and 505 nm (medium-wavelength sensitive). Both in terms of responsivity to lights varying in temporal frequency and in response recovery following intense light adaptation, the cone responses of the pocket gopher are similar to those of other rodents. Labeling experiments indicate an abundance of cones that reach densities in excess of 30,000 mm−2. Cones containing UV opsin are found throughout the retina, but those containing medium-wavelength sensitive opsin are mostly restricted to the dorsal retina where coexpression of the two photopigments is apparently the rule. Rod densities are lower than those typical for nocturnal mammals.


Photoreceptors Thomomys bottae Photopigment coexpression Ultraviolet Electroretinogram 





Long-wavelength sensitive


Medium-wavelength sensitive


Short-wavelength sensitive


Ultraviolet-wavelength sensitive


Outer nuclear layer



We thank John Fenwick for help with the anatomy and Kris Krogh for making the lens measurements. All animal care and experimental procedures were in accordance with institutional care and use guidelines and with the Principles of animal care, publication No. 86–23, revised 1985 of the National Institutes of Health. This research was facilitated by a grant from the National Eye Institute (EY002052).


  1. Adkins RM, Walton AH, Honeycutt RL (2003) Higher-level systematics of rodents and divergence time estimates based on two congruent nuclear genes. Mol Phylogen Evol 26:409–420CrossRefGoogle Scholar
  2. Ahnelt PK, Kolb H (2000) The mammalian photoreceptor mosaic-adaptive design. Prog Retinal Eye Res 19:711–770CrossRefGoogle Scholar
  3. Applebury ML, Antoch MP, Baxter LC, Chun LLY, Falk JD, Farhangfar F, Kage K, Kryzystolik ML, Lyass LA, Robbins JT (2000) The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27:513–523PubMedGoogle Scholar
  4. Arrese CA, Hart NS, Thomas N, Beazley LD, Shand J (2002) Trichromacy in Australian marsupials. Curr Biol 12:657–660CrossRefPubMedGoogle Scholar
  5. Blanks J, Johnson LV (1984) Specific binding of peanut lectin to a class of retinal photoreceptor cells: a species comparison. Invest Ophthalmol Visual Sci 25:546–557Google Scholar
  6. Burda H, Bruns V, Muller M (1989) Sensory adaptations in subterranean mammals. In: Nevo E, Reig OA (eds) Evolution of subterranean mammals at the organismal and molecular levels. Wiley, New York, pp 49–69Google Scholar
  7. Chavez AE, Bozinovic F, Peichl L, Palacios AG (2003) Retinal spectral sensitivity, fur coloration, and urine reflectance in the genus Octodon (Rodentia): implications for visual ecology. Invest Ophthalmol Visual Sci 44:2290–2296CrossRefGoogle Scholar
  8. Chiu MI, Zack DJ, Wang Y, Nathans J (1994) Murine and bovine blue cone pigment genes: cloning and characterization of the S family of visual pigments. Genomics 21:440–443CrossRefPubMedGoogle Scholar
  9. David-Gray ZK, Bellingham J, Munoz M, Avivi A, Nevo E, Foster RG (2002) Adaptive loss of ultraviolet-sensitive/violet-sensitive (UVS/VS) cone opsin in the blind mole rat (Spalax ehrenbergi). Eur Neurosci 15:1186–1194CrossRefGoogle Scholar
  10. Fasick JI, Cronin TW, Hunt DM, Robinson PR (1998) The visual pigments of the bottlenose dolphin (Tursiops truncatus). Visual Neurosci 15:643–651CrossRefGoogle Scholar
  11. Feldman JL, Phillips CJ (1984) Comparative retinal pigment epithelium and photoreceptor ultrastructure in nocturnal and fossorial rodents: the eastern woodrat, Neotoma florida and the plains pocket gopher, Geomys bursarius. J Mammal 65:231–245Google Scholar
  12. Gettinger RD (1984) A field study of activity patterns of Thomomys bottae. J Mammalogy 65:76–84Google Scholar
  13. Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K (2000) In search of the visual pigment template. Visual Neurosci 17:509–528CrossRefGoogle Scholar
  14. Hallett PE (1987) The scale of the visual pathways of mouse and rat. Biol Cybern 57:275–286CrossRefPubMedGoogle Scholar
  15. Hemmi JM, Grunert U (1999) Distribution of photoreceptor types in the retina of a marsupial, the tammar wallaby (Macropus eugenii). Visual Neurosci 16:291–302CrossRefGoogle Scholar
  16. Howland HC, Merola S, Basarab JR (2004) The allometry and scaling of the size of vertebrate eyes. Vision Res 44:2043–2065CrossRefPubMedGoogle Scholar
  17. Hunt DM, Wilkie SE, Bowmaker JK, Poopalasundaram S (2001) Vision in the ultraviolet. Cell Mol Life Sci 58:1583–1598PubMedGoogle Scholar
  18. Jacobs GH (1993) The distribution and nature of colour vision among the mammals. Biol Rev 68:413–471CrossRefPubMedGoogle Scholar
  19. Jacobs GH, Rowe MP (2004) Evolution of vertebrate colour vision. Clin Exp Optom 87(4–5):206–216Google Scholar
  20. Jacobs GH, Neitz J, Deegan II JF (1991) Retinal receptors in rodents maximally sensitive to ultraviolet light. Nature 353:655–656CrossRefPubMedGoogle Scholar
  21. Jacobs GH, Neitz J, Krogh K (1996a) Electroretinogram flicker photometry and its applications. J Opt Soc Am A 13:641–648Google Scholar
  22. Jacobs GH, Neitz M, Neitz J (1996b) Mutations in S-cone pigment genes and the absence of colour vision in two species of nocturnal primate. Proc R Soc Lond B 263:705–710PubMedGoogle Scholar
  23. Jacobs GH, Fenwick JC, Calderone JB, Deeb SS (1999) Human cone pigment expressed in transgenic mice yields altered vision. J Neurosci 19:3258–3265PubMedGoogle Scholar
  24. Jacobs GH, Calderone JB, Fenwick JA, Krogh K, Williams GA (2003) Visual adaptations in a diurnal rodent, Octodon degus. J Comp Physiol A 189:347–361Google Scholar
  25. Jeon C-J, Strettoi E, Masland RH (1998) The major cell populations of the mouse retina. J Neurosci 18:8936–8946PubMedGoogle Scholar
  26. Kawamura S, Kubotera N (2004) Ancestral loss of short wave-sensitive cone visual pigment in lorsiform prosiminans, contrasting with its strict conservation in other prosimians. J Mol Evol 58(3):314–321CrossRefPubMedGoogle Scholar
  27. Kryger Z, Galli-Resta L, Jacobs GH, Reese BE (1998) The topography of rod and cone photoreceptors in the retina of the ground squirrel. Visual Neurosci 15:685–691CrossRefGoogle Scholar
  28. Laughlin SB (2001) Energy as a constraint on the coding and processing of sensory information. Curr Opin Neurobiol 11:475–480CrossRefPubMedGoogle Scholar
  29. Levenson DH, Dizon A (2003) Genetic evidence for the ancestral loss of SWS cone pigments in mysticetee and odontocete cetaceans. Proc R Soc Lond B 270:673–679CrossRefPubMedGoogle Scholar
  30. Macdonald D (ed) (2001) The new encyclopedia of mammals. Oxford University Press, OxfordGoogle Scholar
  31. Nowak RM (1991) Walker’s mammals of the world. Johns Hopkins University Press, BaltimoreGoogle Scholar
  32. Parry JWL, Bowmaker JK (2002) Visual pigment coexpression in guinea pig cones: a microspectrophotometric study. Invest Ophthalmol Visual Sci 43:1662–1665Google Scholar
  33. Paupoo AAV, Mahroo OAR, Friedburg C, Lamb TD (2000) Human cone photoreceptor responses measured by the electroretinogram a-wave during and after exposure to intense illumination. J Physiol 529:469–482CrossRefPubMedGoogle Scholar
  34. Peichl L, Behrmann G, Kroger RHH (2001) For whales and seals the ocean is not blue: a visual pigment loss in marine mammals. Eur J Neurosci 13:1520–1528CrossRefPubMedGoogle Scholar
  35. Reichman OJ, Seabloom EW (2002) The role of pocket gophers as subterranean ecosystem engineers. Trends Ecol Evol 17:44–49CrossRefGoogle Scholar
  36. Rohlich P, van Veen T, Szel A (1994) Two different visual pigments in one retinal cone cell. Neuron 13:1159–1166CrossRefPubMedGoogle Scholar
  37. Sanyal S, Jansen HG, de Grip WJ, Nevo E, de Jong WW (1990) The eye of the blind mole rat, Spalax ehrenbergi. Rudiment with hidden function? Invest Ophthalmol Visual Sci 31:1398–1404Google Scholar
  38. Shi Y, Yokoyama S (2003) Molecular analysis of the evolutionary significance of ultraviolet vision in vertebrates. Proc Natl Acad Sci U S A 100:8308–8333CrossRefPubMedGoogle Scholar
  39. Smith MF (1998) Phylogenetic relationships and geographic structure in pocket gophers in the genus Thomomys. Mol Phylogenet Evol 9:1–14CrossRefPubMedGoogle Scholar
  40. Sterling P (2004) How retinal circuits optimize the transfer of visual information. In: Chalupa LM, Werner JS (eds) The visual neurosciences, vol 1. MIT Press, Boston, pp 234–259Google Scholar
  41. Szel A, Lukats A, Fekete T, Szepessy Z, Rohlich P (2000) Photoreceptor distribution in the retinas of subprimate mammals. J Opt Soc Am A 17:568–579Google Scholar
  42. Walls GL (1942) The vertebrate eye and its adaptive radiation. Cranbrook Institute of Science, Bloomfield HillsGoogle Scholar
  43. Williams GA, Calderone JB, Jacobs GH (2003) Photoreceptors and photopigments in a fossorial rodent, the Pocket gopher (Thomomys bottae). Invest Ophthalmol Visual Sci 44:4163 (E-Abstract)CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Gary A. Williams
    • 1
  • Jack B. Calderone
    • 1
  • Gerald H. Jacobs
    • 1
    Email author
  1. 1.Neuroscience Research Institute and Department of PsychologyUniversity of CaliforniaSanta BarbaraUSA

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