Topographic analyses of retinal ganglion cell density are very useful in providing information about the visual ecology of a species by identifying areas of acute vision within the visual field (i.e. areas of high cell density). In this study, we investigated the neural cell distribution in the ganglion cell layer of a range of lanternfish species belonging to 10 genera. Analyses were performed on wholemounted retinas using stereology. Topographic maps were constructed of the distribution of all neurons and both ganglion and amacrine cell populations in 5 different species from Nissl-stained retinas using cytological criteria. Amacrine cell distribution was also examined immunohistochemically in 2 of the 5 species using anti-parvalbumin antibody. The distributions of both the total neuron and the amacrine cell populations were aligned in all of the species examined, showing a general increase in cell density toward the retinal periphery. However, when the ganglion cell population was topographically isolated from the amacrine cell population, which comprised up to 80% of the total neurons within the ganglion cell layer, a different distribution was revealed. Topographic maps of the true ganglion cell distribution in 18 species of lanternfishes revealed well-defined specializations in different regions of the retina. Different species possessed distinct areas of high ganglion cell density with respect to both peak density and the location and/or shape of the specialized acute zone (i.e. elongated areae ventro-temporales, areae temporales and large areae centrales). The spatial resolving power was calculated to be relatively low (varying from 1.6 to 4.4 cycles per degree), indicating that myctophids may constitute one of the less visually acute groups of deep-sea teleosts. The diversity in retinal specializations and spatial resolving power within the family is assessed in terms of possible ecological functions and evolutionary history.

1.
Baddeley A, Turner R (2005): Spatstat: an R package for analyzing spatial point patterns. J Stat Softw 12:1-42.
2.
Bailes HJ, Robinson SR, Trezise AEO, Collin SP (2006a): Morphology, characterization, and distribution of retinal photoreceptors in the Australian lungfish Neoceratodus forsteri (Krefft, 1870). J Comp Neurol 494:381-397.
3.
Bailes HJ, Trezise AEO, Collin SP (2006b): The number, morphology, and distribution of retinal ganglion cells and optic axons in the Australian lungfish Neoceratodus forsteri (Krefft 1870). Vis Neurosci 23:257-273.
4.
Ball AK, Dickson DH (1983): Displaced amacrine and ganglion cells in the newt retina. Exp Eye Res 36:199-213.
5.
Bozzano A, Catalán I (2002): Ontogenetic changes in the retinal topography of the European hake, Merluccius merluccius: implications for feeding and depth distribution. Mar Biol 141:549-559.
6.
Bozzano A, Collin SP (2000): Retinal ganglion cell topography in elasmobranchs. Brain Behav Evol 55:191-208.
7.
Bozzano A, Pankhurst PM, Sabatés A (2007): Early development of eye and retina in lanternfish larvae. Vis Neurosci 24:423-436.
8.
Case JF, Warner J, Barnes AT, Lowenstine M (1977): Bioluminescence of lantern fish (Myctophidae) in response to changes in light intensity. Nature 265:179-181.
9.
Casini G, Rickman DW, Brecha NC (1995): AII amacrine cell population in the rabbit retina: identification by parvalbumin immunoreactivity. J Comp Neurol 356:132-142.
10.
Coimbra JP, Hart NS, Collin SP, Manger PR (2013): Scene from above: retinal ganglion cell topography and spatial resolving power in the giraffe (Giraffa camelopardalis). J Comp Neurol 521:2042-2057.
11.
Coimbra JP, Marceliano MLV, Andrade-da-Costa BLS, Yamada ES (2006): The retina of tyrant flycatchers: topographic organization of neuronal density and size in the ganglion cell layer of the great kiskadee Pitangus sulphuratus and the rusty margined flycatcher Myiozetetes cayanensis (aves: Tyrannidae). Brain Behav Evol 68:15-25.
12.
Coimbra JP, Nolan PM, Collin SP, Hart NS (2012): Retinal ganglion cell topography and spatial resolving power in penguins. Brain Behav Evol 80:254-268.
13.
Coimbra JP, Trévia N, Marceliano MLV, Andrade-Da-Costa BLS, Picanço-Diniz CW, Yamada ES (2009): Number and distribution of neurons in the retinal ganglion cell layer in relation to foraging behaviors of tyrant flycatchers. J Comp Neurol 514:66-73.
14.
Collin SP (1997): Specialisations of the teleost visual system: adaptive diversity from shallow-water to deep-sea. Acta Physiol Scand Suppl 638:5-24.
15.
Collin S (1988): The retina of the shovel-nosed ray, Rhinobatos batillum (Rhinobatidae): morphology and quantitative analysis of the ganglion, amacrine and bipolar cell populations. J Exp Biol 47:195-207.
16.
Collin SP (2008): A web-based archive for topographic maps of retinal cell distribution in vertebrates. Clin Exp Optom 91:85-95.
17.
Collin SP, Hoskins RV (1997): Topographic mismatching of the displaced amacrine and ganglion cell populations in the retina of deep-sea lanternfish. Soc Neurosci Abstr 23:729.
18.
Collin SP, Hoskins RV, Partridge JC (1997): Tubular eyes of deep-sea fishes: a comparative study of retinal topography. Brain Behav Evol 50:335-357.
19.
Collin SP, Hoskins RV, Partridge JC (1998): Seven retinal specializations in the tubular eye of the deep-sea pearleye, Scopelarchus michaelsarsi: a case study in visual optimization. Brain Behav Evol 51:291-314.
20.
Collin SP, Lloyd DJ, Wagner H-J (2000): Foveate vision in deep-sea teleosts: a comparison of primary visual and olfactory inputs. Philosophic Trans R Soc Lond B Biol Sci 355:1315-1320.
21.
Collin SP, Partridge JC (1996): Retinal specializations in the eyes of deep-sea teleosts. J Fish Biol 49:157-174.
22.
Collin SP, Pettigrew JD (1988a): Retinal topography in reef teleosts. 1. Some species with well-developed areae but poorly-developed streaks. Brain Behav Evol 31:269-282.
23.
Collin SP, Pettigrew JD (1988b): Retinal topography in reef teleosts. 2. Some species with prominent horizontal streaks and high-density areae. Brain Behav Evol 31:283-295.
24.
Collin SP, Pettigrew JD (1988c): Retinal ganglion cell topography in teleosts: a comparison between Nissl-stained material and retrograde labelling from the optic nerve. J Comp Neurol 276:412-422.
25.
Collin SP, Pettigrew JD (1989): Quantitative comparison of the limits on visual spatial resolution set by the ganglion cell layer in twelve species of reef teleosts. Brain Behav Evol 34:184-192.
26.
Collin SP, Shand J (2003): Retinal sampling and the visual field in fishes; in Collin SP, Marshall NJ (eds): Sensory Processing in Aquatic Environments. New York, Springer, pp 139-169.
27.
de Busserolles F, Fitzpatrick JL, Marshall NJ, Collin SP (2014b): The influence of photoreceptor size and distribution on optical sensitivity in the eyes of lanternfishes (Myctophida). PLoS One 9:e99957.
28.
de Busserolles F, Fitzpatrick JL, Paxton JR, Marshall NJ, Collin SP (2013): Eye-size variability in deep-sea lanternfishes (Myctophidae): an ecological and phylogenetic study. PLoS One 8:e58519.
29.
de Busserolles F, Marshall NJ, Collin SP (2014a): The eyes of lanternfishes (Myctophidae, teleostei): novel ocular specialisations for vision in dim light. J Comp Neurol 522:1618-1640.
30.
Edwards AS, Herring PJ (1977): Observations on the comparative morphology and operation of the photogenic tissues of myctophid fishes. Mar Biol 41:59-70.
31.
Fritsches KA, Marshall NJ, Warrant EJ (2003): Retinal specializations in the blue marlin: eyes designed for sensitivity to low light levels. Mar Freshw Res 54:333-341.
32.
Gabriel R, Straznicky C (1992): Immunocytochemical localization of parvalbumin- and neurofilament triplet protein immunoreactivity in the cat retina: colocalization in a subpopulation of AII amacrine cells. Brain Res 595:133-136.
33.
Garza-Gisholt E, Hemmi JM, Hart NS, Collin SP (2014): A comparison of spatial analysis methods for the construction of topographic maps of retinal cell density. PLoS One 9:e93485.
34.
Glaser EM, Wilson PD (1998): The coefficient of error of optical fractionator population size estimates: a computer simulation comparing three estimators. J Microsc 192:163-171.
35.
Haddock SHD, Moline MA, Case JF (2010): Bioluminescence in the sea. Annu Rev Mar Sci 2:443-493.
36.
Herring PJ (1985): How to survive in the dark: bioluminescence in the deep sea. Symp Soc Exp Biol 39:323-350.
37.
Herring PJ (2002): The Biology of the Deep-Sea. New York, Oxford University Press.
38.
Herring PJ (2007): Sex with the lights on? A review of bioluminescent sexual dimorphism in the sea. J Mar Biol Assoc UK 87:829-842.
39.
Hughes A (1975): A quantitative analysis of the cat retinal ganglion cell topography. J Comp Neurol 163:107-128.
40.
Hughes A (1977): The topography of vision in mammals of contrasting life style: comparative optics and retinal organisation; in Crescitelli F (ed): Handbook of Sensory Physiology. Berlin, Springer, vol II/5, pp 613-756.
41.
Jeon YK, Kim TJ, Lee JY, Choi JS, Jeon CJ (2007): AII amacrine cells in the inner nuclear layer of bat retina: identification by parvalbumin immunoreactivity. Neuroreport 18:1095-1099.
42.
Karnella C (1987): Family Myctophidae, lanternfishes; in Gibbs RH, Krueger WH (eds): Biology of Midwater Fishes of the Bermuda Ocean Acre. Washington, Smithsonian Institution Press, pp 51-168.
43.
Kristoffersen JB, Salvanes AGV (1998): Effects of formaldehyde and ethanol preservation on body and otoliths of Maurolicus muelleri and Benthosema glaciale. Sarsia 83:95-102.
44.
Locket NA (1977): Adaptations to the deep-sea environment; in Crescitelli F (ed): Handbook of Sensory physiology. Springer, Berlin, vol II/5, pp 67-192.
45.
Mack AF, Sussmann C, Hirt B, Wagner HJ (2004): Displaced amacrine cells disappear from the ganglion cell layer in the central retina of adult fish during growth. Invest Ophthalmol Vis Sci 45:3749-3755.
46.
Matthiessen L (1882): Über die Beziehungen, welche zwischen dem Brechungsindex des Kernzentrums der Krystalllinse und den Dimensionen des Auges bestehen. Pflügers Arch 27:510-523.
47.
Matthiessen L (1886): Über den physikalisch-optischen Bau des Auges der Cetacean und der Fische. Pflügers Arch 38:521-528.
48.
Moser HG, Ahlstrom EH (1970): Development of lanternfishes (family Myctophidae) in the California Current. 1. Species with narrow-eyed larvae. Nat Hist Mus Los Angel Cty Sci Bull 7:1-145.
49.
Moser HG, Ahlstrom EH (1972): Development of lanternfish, Scopelopsis multipunctatus Brauer 1906, with a discussion of its phylogenetic position in the family Myctophidae and its role in a proposed mechanism for the evolution of photophore patterns in lanternfishes. Fish Bull 70:541-564.
50.
Moser HG, Ahlstrom EH (1974): Role of larval stages in systematic investigations of marine teleosts: the Myctophidae, a case study. Fish Bull 72:391-413.
51.
Nafpaktitis BG (1978): Systematics and distribution of lanternfishes of the genera Lobianchia and Diaphus (Myctophidae) in the Indian Ocean. Nat Hist Mus Los Angel Cty Sci Bull 30:1-92.
52.
Nafpaktitis BG, Backus RH, Craddock JE, Haedrich RL, Robison BH, Karnella C (1977): Family Myctophidae; in Gibbs RH Jr, Berry FH, Böhlke JE, Cohen DM, Collette BB, Eschmeyer WN, Mead GW, Merriman D, Pietsch TW (eds): Fishes of the Western North Atlantic - Memoir of the Sears Foundation for Marine Research. New Haven, Yale University, vol 1, pp 13-265.
53.
Nafpaktitis BG, Nafpaktitis M (1969): Lanternfishes (family Myctophidae) collected during cruises 3 and 6 of the R/V Anton Bruun in the Indian Ocean. Nat Hist Mus Los Angel Cty Sci Bull 5:1-79.
54.
Nelson R (1982): AII amacrine cells quicken time course of rod signals in the cat retina. J Neurophysiol 47:928-947.
55.
Paxton JR (1972): Osteology and relationships of the lanternfishes (family Myctophidae). Nat Hist Mus Los Angel Cty Sci Bull 13:1-81.
56.
Paxton JR, Ahlstrom EH, Moser HG (1984): Myctophidae: relationships; in Moser HG, Richards WJ, Cohen DM, Fahay MP, Kendall AW, Richerdson SL (eds): Ontogeny and Systematic of Fishes. La Jolla, American Society of Ichthyologists and Herpetologists, vol 1, pp 239-244.
57.
Podrazhanskaya SG (1993): Feeding habits of mesopelagic species of fish and estimation of plankton graze in the northwest Atlantic. Sci Counc Stud NAFO 19:79-85.
58.
Slomianka L, West MJ (2005): Estimators of the precision of stereological estimates: an example based on the CA1 pyramidal cell layer of rats. Neurosci 136:757-767.
59.
Stone J (1981): The Whole Mount Handbook: a Guide to the Preparation and Analysis of Retinal Whole Mounts. Sydney, Maitland.
60.
Stone J (1983): Parallel processing in the visual system. New York, Plenum Press, p 438.
61.
Ullmann JFP, Moore BA, Temple SE, Fernandez-Juricic E, Collin SP (2011): The retinal wholemount technique: a window to understanding the brain and behaviour. Brain Behav Evol 79:26-44.
62.
Vaney DI, Peichl L, Boycott BB (1981): Matching populations of amacrine cells in the inner nuclear and ganglion cell layers of the rabbit retina. J Comp Neurol 199:373-391.
63.
van Haesendonck E, Missotten L (1987): Displaced small amacrine cells in the retina of the marine teleost Callionymus lyra L. Vision Res 27:1431-1443.
64.
Wagner H-J (2001): Sensory brain areas in mesopelagic fishes. Brain Behav Evol 57:117-133.
65.
Wagner H-J, Fröhlich E, Negishi K, Collin SP (1998): The eyes of deep-sea fish. 2. Functional morphology of the retina. Prog Retin Eye Res 17:637-685.
66.
Wagner H, Wagner E (1988): Amacrine cells in the retina of a teleost fish, the roach (Rutilus rutilus): a Golgi study on differentiation and layering. Phil Trans R Soc Lond B Biol Sci 321:263-324.
67.
Walls GL (1942): The vertebrate eye and its adaptive radiation. Bloomfield Hills, The Cranbrook Institute of Science.
68.
Wässle H, Grünert U, Röhrenbeck J (1993): Immunocytochemical staining of AII-amacrine cells in the rat retina with antibodies against parvalbumin. J Comp Neurol 332:407-420.
69.
Watanabe H, Moku M, Kawaguchi K, Ishimaru K, Ohno A (1999): Diel vertical migration of myctophid fishes (family Myctophidae) in the transitional waters of the western North Pacific. Fish Oceanogr 8:115-127.
70.
Weruaga E, Velasco A, Brinon JG, Arevalo R, Aijon J, Alonso JR (2000): Distribution of the calcium-binding proteins parvalbumin, calbindin D-28k and calretinin in the retina of two teleosts. J Chem Neuroanat 19:1-15.
71.
West MJ, Slomianka L, Gundersen HJG (1991): Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
72.
Wong ROL, Hughes A (1987): The morphology, number, and distribution of a large population of confirmed displaced amacrine cells in the adult cat retina. J Comp Neurol 255:159-177.
73.
Zahuranec BJ (2000): Zoogeography and systematics of the lanternfishes of the genus Nannobrachium (Myctophidae: Lampanyctini). Smithson Contrib Zool 607:1-69.
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