The visual ecology of Holocentridae, a nocturnal coral reef fish family with a deep-sea-like multibank retina

The visual systems of teleost fishes usually match their habitats and lifestyles. Since coral reefs are bright and colourful environments, the visual systems of their diurnal inhabitants have been more extensively studied than those of nocturnal species. In order to fill this knowledge gap, we conducted a detailed investigation of the visual system of the nocturnal reef fish family Holocentridae. Results showed that the visual system of holocentrids is well adapted to their nocturnal lifestyle with a rod-dominated retina. Surprisingly, rods in all species were arranged into 6-17 well-defined banks, a feature most commonly found in deep-sea fishes, that may increase the light sensitivity of the eye and/or allow colour discrimination in dim-light. Holocentrids also have the potential for dichromatic colour vision during the day with the presence of at least two spectrally different cone types: single cones expressing the blue-sensitive SWS2A gene, and double cones expressing one or two green-sensitive RH2 genes. Some differences were observed between the two subfamilies, with Holocentrinae (squirrelfish) having a slightly more developed photopic visual system than Myripristinae (soldierfish). Moreover, retinal topography of both ganglion cells and cone photoreceptors showed specific patterns for each cell type, likely highlighting different visual demands at different times of the day, such as feeding. Overall, their well-developed scotopic visual systems and the ease of catching and maintaining holocentrids in aquaria, make them ideal models to investigate teleost dim-light vision and more particularly shed light on the function of the multibank retina and its potential for dim-light colour vision.

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The visual ecology of Holocentridae, a nocturnal coral reef fish family with a deep-sea-like multibank retina

10.1101/2020.05.24.113811 ◽

2020 ◽

Author(s):

Fanny de Busserolles ◽

Fabio Cortesi ◽

Lily Fogg ◽

Sara M. Stieb ◽

Martin Luerhmann ◽

...

Keyword(s):

Coral Reef ◽

Visual System ◽

Reef Fish ◽

Coral Reef Fish ◽

Deep Sea ◽

Colour Vision ◽

Fish Family ◽

Visual Systems ◽

Dim Light ◽

Dim Light Vision

AbstractThe visual systems of teleost fishes usually match their habitats and lifestyles. Since coral reefs are bright and colourful environments, the visual systems of their diurnal inhabitants have been more extensively studied than those of nocturnal species. In order to fill this knowledge gap, we conducted a detailed investigation of the visual systems of the coral reef fish family Holocentridae (squirrelfish and soldierfish). In addition to their nocturnality, this family is particularly interesting for dim-light vision studies due to its ecological and evolutionary connection to deeper habitats. Results showed that the visual system of holocentrids is well adapted to their nocturnal lifestyle with a rod-dominated retina. Surprisingly, rods in all species were arranged into 6-17 well-defined banks, a feature most commonly found in deep-sea fishes, that may increase the light sensitivity of the eye and/or allow colour discrimination in dim-light. Holocentrids also have the potential for dichromatic colour vision during the day with the presence of at least two spectrally different cone types: single cones expressing the blue-sensitive SWS2A gene, and double cones expressing one or two green-sensitive RH2 genes. Some differences were observed between the two subfamilies, with Holocentrinae having a slightly more developed photopic visual system than Myripristinae. Moreover, retinal topography of both ganglion cells and cone photoreceptors showed specific patterns for each cell type, likely highlighting different visual demands at different times of the day, such as feeding. Overall, their well-developed scotopic visual systems and the ease of catching and maintaining holocentrids in aquaria, make them ideal models to investigate teleost dim-light vision and more particularly shed light on the function of multibank retina and its potential for dim-light colour vision.

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Ontogenetic adaptations in the visual systems of deep-sea crustaceans

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0071 ◽

2017 ◽

Vol 372 (1717) ◽

pp. 20160071 ◽

Cited By ~ 3

Author(s):

Tamara M. Frank

Keyword(s):

Temporal Resolution ◽

Deep Sea ◽

Life Histories ◽

Marine Species ◽

Light Regime ◽

Life History Stages ◽

Visual Systems ◽

Juvenile Stages ◽

Dim Light ◽

Effects Of Temperature

For all visually competent organisms, the driving force behind the adaptation of photoreceptors involves obtaining the best balance of resolution to sensitivity in the prevailing light regime, as an increase in sensitivity often results in a decrease in resolution. A number of marine species have an additional problem to deal with, in that the juvenile stages live in relatively brightly lit shallow (100–200 m depth) waters, whereas the adult stages have daytime depths of more than 600 m, where little downwelling light remains. Here, I present the results of electrophysiological analyses of the temporal resolution and irradiance sensitivity of juvenile and adult stages of two species of ontogenetically migrating crustaceans ( Gnathophausia ingens and Systellaspis debilis ) that must deal with dramatically different light environments and temperatures during their life histories. The results demonstrate that there are significant effects of temperature on temporal resolution, which help to optimize the visual systems of the two life-history stages for their respective light environments. This article is part of the themed issue ‘Vision in dim light’.

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Colour Perception 1978–1997

Perception ◽

10.1068/v970021 ◽

1997 ◽

Vol 26 (1_suppl) ◽

pp. 274-274

Author(s):

J D Mollon

Keyword(s):

Visual System ◽

Dna Sequences ◽

Colour Vision ◽

Ganglion Cells ◽

Major Change ◽

Natural Scenes ◽

Colour Perception ◽

Cone Pigments ◽

The Status ◽

Opponent Processes

In the past twenty years, the spectral sensitivities of the three types of cone have been established with some certainty: direct measurements by microspectrophotometry and electrophysiology are in fair agreement with psychophysical estimates. Particularly significant was the publication of DNA sequences for the four opsins of the human eye, by Jeremy Nathans and colleagues in 1986. This work was soon to transform the understanding of retinitis pigmentosa and other retinal dystrophies, and it has given many insights into the evolution of colour vision; but, curiously, the explanations of dichromacy and anomalous trichromacy have not proved as straightforward as we all expected in 1986. What is clear, however, is that normal colour vision exhibits a genetic polymorphism: much of the intersubject variance in colour matches can be traced to differences in the amino-acid sequence of the opsins for the long-wave and middle-wave cone pigments. The last two decades have seen a major change in the status of opponent processes. In the 1970s it was still common for professors to tell undergraduates that the Young - Helmholtz theory of colour vision held at the receptor level and the Hering theory at the level of the retinal ganglion cells. It is now clear that the chromatically antagonistic processes revealed electrophysiologically and psychophysically in the early visual system do not correspond to the red - green and yellow - blue processes that Hering postulated on the basis of phenomenological observations. The existence of four unique hues is today one of the unexplained mysteries of colour science. In one salient respect, research in colour vision has been changed by instrumental advances. Computer-controlled monitors (though offering splendid pitfalls to the unwary) have allowed the study of spatially and temporally complex chromatic displays, notably in the field of colour constancy. Most recently there has been interest in the chromatic statistics of natural scenes: how well is the visual system matched to the statistics of the world and can it adapt to the gamut of chromaticities present in a given scene?

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Divergent photic thresholds in the non-image-forming visual system: entrainment, masking and pupillary light reflex

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2010.1509 ◽

2010 ◽

Vol 278 (1706) ◽

pp. 745-750 ◽

Cited By ~ 32

Author(s):

Matthew P. Butler ◽

Rae Silver

Keyword(s):

Visual System ◽

Wheel Running ◽

Ganglion Cells ◽

Animal Husbandry ◽

Pupillary Light Reflex ◽

Photon Flux ◽

Light Reflex ◽

Pupillary Light ◽

Circadian Timing System ◽

Dim Light

Light is the principal cue that entrains the circadian timing system, but the threshold of entrainment and the relative contributions of the retinal photoreceptors—rods, cones and intrinsically photosensitive retinal ganglion cells—are not known. We measured thresholds of entrainment of wheel-running rhythms at three wavelengths, and compared these to thresholds of two other non-image-forming visual system functions: masking and the pupillary light reflex (PLR). At the entrainment threshold, the relative spectral sensitivity and absolute photon flux suggest that this threshold is determined by rods. Dim light that entrained mice failed to elicit either masking or PLR; in general, circadian entrainment is more sensitive by 1–2 log units than other measures of the non-image-forming visual system. Importantly, the results indicate that dim light can entrain circadian rhythms even when it fails to produce more easily measurable acute responses to light such as phase shifting and melatonin suppression. Photosensitivity to one response, therefore, cannot be generalized to other non-image-forming functions. These results also impact practical problems in selecting appropriate lighting in laboratory animal husbandry.

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Seeing in the deep-sea: visual adaptations in lanternfishes

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0070 ◽

2017 ◽

Vol 372 (1717) ◽

pp. 20160070 ◽

Cited By ~ 18

Author(s):

Fanny de Busserolles ◽

N. Justin Marshall

Keyword(s):

Visual System ◽

Deep Sea ◽

Extreme Environment ◽

Ambient Light ◽

Body Of Knowledge ◽

Mesopelagic Zone ◽

The World ◽

Dim Light

Ecological and behavioural constraints play a major role in shaping the visual system of different organisms. In the mesopelagic zone of the deep- sea, between 200 and 1000 m, very low intensities of downwelling light remain, creating one of the dimmest habitats in the world. This ambient light is, however, enhanced by a multitude of bioluminescent signals emitted by its inhabitants, but these are generally dim and intermittent. As a result, the visual system of mesopelagic organisms has been pushed to its sensitivity limits in order to function in this extreme environment. This review covers the current body of knowledge on the visual system of one of the most abundant and intensely studied groups of mesopelagic fishes: the lanternfish (Myctophidae). We discuss how the plasticity, performance and novelty of its visual adaptations, compared with other deep-sea fishes, might have contributed to the diversity and abundance of this family. This article is part of the themed issue ‘Vision in dim light’.

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The visual ecology of a deep-sea fish, the escolar Lepidocybium flavobrunneum (Smith, 1843)

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2013.0039 ◽

2014 ◽

Vol 369 (1636) ◽

pp. 20130039 ◽

Cited By ~ 9

Author(s):

Eva Landgren ◽

Kerstin Fritsches ◽

Richard Brill ◽

Eric Warrant

Keyword(s):

Surface Waters ◽

Deep Sea ◽

Ganglion Cells ◽

Optical Path Length ◽

Predatory Fish ◽

Flicker Fusion Frequency ◽

Optical Sensitivity ◽

Light Levels ◽

Electrophysiological Recordings ◽

Maximal Absorption

Escolar ( Lepidocybium flavobrunneum , family Gempylidae) are large and darkly coloured deep-sea predatory fish found in the cold depths (more than 200 m) during the day and in warm surface waters at night. They have large eyes and an overall low density of retinal ganglion cells that endow them with a very high optical sensitivity. Escolar have banked retinae comprising six to eight layers of rods to increase the optical path length for maximal absorption of the incoming light. Their retinae possess two main areae of higher ganglion cell density, one in the ventral retina viewing the dorsal world above (with a moderate acuity of 4.6 cycles deg −1 ), and the second in the temporal retina viewing the frontal world ahead. Electrophysiological recordings of the flicker fusion frequency (FFF) in isolated retinas indicate that escolar have slow vision, with maximal FFF at the highest light levels and temperatures (around 9 Hz at 23°C) which fall to 1–2 Hz in dim light or cooler temperatures. Our results suggest that escolar are slowly moving sit-and-wait predators. In dim, warm surface waters at night, their slow vision, moderate dorsal resolution and highly sensitive eyes may allow them to surprise prey from below that are silhouetted in the downwelling light.

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The visual system of a Palaeognathous bird: Visual field, retinal topography and retino-central connections in the Chilean Tinamou (Nothoprocta perdicaria)

The Journal of Comparative Neurology ◽

10.1002/cne.23676 ◽

2014 ◽

Vol 523 (2) ◽

pp. 226-250 ◽

Cited By ~ 6

Author(s):

Quirin Krabichler ◽

Tomas Vega-Zuniga ◽

Cristian Morales ◽

Harald Luksch ◽

Gonzalo J. Marín

Keyword(s):

Visual Field ◽

Visual System ◽

Retinal Topography ◽

Nothoprocta Perdicaria

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Thresholds and noise limitations of colour vision in dim light

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0065 ◽

2017 ◽

Vol 372 (1717) ◽

pp. 20160065 ◽

Cited By ~ 25

Author(s):

Almut Kelber ◽

Carola Yovanovich ◽

Peter Olsson

Keyword(s):

Shot Noise ◽

Colour Vision ◽

Absolute Threshold ◽

Colour Discrimination ◽

Dark Noise ◽

Visual Threshold ◽

Light Intensities ◽

Purkinje Shift ◽

Dim Light ◽

Receptor Noise

Colour discrimination is based on opponent photoreceptor interactions, and limited by receptor noise. In dim light, photon shot noise impairs colour vision, and in vertebrates, the absolute threshold of colour vision is set by dark noise in cones. Nocturnal insects (e.g. moths and nocturnal bees) and vertebrates lacking rods (geckos) have adaptations to reduce receptor noise and use chromatic vision even in very dim light. In contrast, vertebrates with duplex retinae use colour-blind rod vision when noisy cone signals become unreliable, and their transition from cone- to rod-based vision is marked by the Purkinje shift. Rod–cone interactions have not been shown to improve colour vision in dim light, but may contribute to colour vision in mesopic light intensities. Frogs and toads that have two types of rods use opponent signals from these rods to control phototaxis even at their visual threshold. However, for tasks such as prey or mate choice, their colour discrimination abilities fail at brighter light intensities, similar to other vertebrates, probably limited by the dark noise in cones. This article is part of the themed issue 'Vision in dim light’.

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Expression of the BDNF gene in the developing visual system of the chick

Development ◽

10.1242/dev.120.6.1643 ◽

1994 ◽

Vol 120 (6) ◽

pp. 1643-1649 ◽

Cited By ~ 4

Author(s):

K.H. Herzog ◽

K. Bailey ◽

Y.A. Barde

Keyword(s):

Visual System ◽

Ganglion Cells ◽

Mrna Levels ◽

Retinal Ganglion ◽

Bdnf Gene ◽

Bdnf Mrna ◽

Optic Stalk ◽

Copy Numbers ◽

Activity Dependent

Using a sensitive and quantitative method, the mRNA levels of brain-derived neurotrophic factor (BDNF) were determined during the development of the chick visual system. Low copy numbers were detected, and BDNF was found to be expressed in the optic tectum already 2 days before the arrival of the first retinal ganglion cell axons, suggesting an early role of BDNF in tectal development. After the beginning of tectal innervation, BDNF mRNA levels markedly increased, and optic stalk transection at day 4 (which prevents subsequent tectal innervation) was found to reduce the contralateral tectal levels of BDNF mRNA. Comparable reductions were obtained after injection of tetrodotoxin into one eye, indicating that, already during the earliest stages of target encounter in the CNS, the degree of BDNF gene expression is influenced by activity-dependent mechanisms. BDNF mRNA was also detected in the retina itself and at levels comparable to those found in the tectum. Together with previous findings indicating that BDNF prevents the death of cultured chick retinal ganglion cells, these results support the idea that the tightly controlled expression of the BDNF gene might be important in the co-ordinated development of the visual system.

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