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Dryad

Multiple rod layers increase the speed and sensitivity of vision in nocturnal reef fishes

Cite this dataset

Fogg, Lily G. et al. (2023). Multiple rod layers increase the speed and sensitivity of vision in nocturnal reef fishes [Dataset]. Dryad. https://doi.org/10.5061/dryad.280gb5mtf

Abstract

Most vertebrates have one layer of the dim-light active rod photoreceptors. However, multiple rod layers, known as a multibank retina, can be found in over 100 species of fish, including several deep-sea species and one family of nocturnally active reef fish, the Holocentridae. Although seemingly associated with increased photon catch, the function of multibank retinas remained unknown. We used an integrative approach, combining histology, electrophysiology, and amino acid sequence analysis, applied to three species of nocturnal reef fishes, two holocentrids with a multibank retina (Neoniphon sammara and Myripristis violacea) and an apogonid with a single rod bank (Ostorhinchus compressus), to determine the sensory advantage of multiple rod layers. Our results showed that fish with multibank retinas have both faster vision and enhanced sensitivity to bright and dim light intensities. Faster vision was indicated by higher flicker fusion frequencies during temporal resolution electroretinography as well as faster retinal release kinetics estimated from their rhodopsin proteins. Enhanced sensitivity was demonstrated by broadened intensity-response curves derived from luminous sensitivity electroretinography. Overall, our findings provide the first functional evidence for enhanced dim-light sensitivity using a multibank retina while also suggesting novel roles for the adaptation in enhancing bright-light sensitivity and the speed of vision.

README

This README.md file is for he dataset "Multiple rod layers increase the speed and sensitivity of vision in nocturnal reef fishes"
The associated preprint can be accessed at: https://www.biorxiv.org/content/10.1101/2022.11.27.518067v1
Dataset Contributors: Lily Fogg, Wen-Sung Chung, N. Justin Marshall, Fabio Cortesi, Fanny de Busserolles
Date Created: 2023.02.09
Date Updated: 2023.10.03

License: Use of these data is covered by the CC0 license

Contact Information
Name:
Affiliations: Queensland Brain Institute
University: University of Queensland, Brisbane, Australia
ORCID ID: 0000-0002-5378-8781
Email: lily.fogg@uqconnect.edu.au
Alternate Email: lily.fogg@unibas.ch
Address: e-mail preferred


Additional dataset metadata

Format

All data files are given as tsv or csv files (file type is indicated in the description of individual data files below). All files can be opened in Microsoft Excel or an alternative non-proprietary software. No unpacking of the data is required. Note that any blank fields have been replaced with NA.

Animal collection and ethics

Adult fish were collected from the Great Barrier Reef around Lizard Island, Australia or sourced from a supplier, Cairns Marine, which also collects from the northern Great Barrier Reef. All collections and procedures were conducted under a Great Barrier Reef Marine Park Permit (G17/38160.1), a Queensland General Fisheries Permit (180731), and a University of Queensland’s Animal Ethics Permit (QBI 304/16). Following euthanasia, all animals were photographed with a scale reference to quantify body length and eye diameter. Eyes were dissected and the eye cup preserved in RNAlater or paraformaldehyde [PFA; 4% (w/v) PFA in 0.01M phosphate-buffered saline (PBS), pH 7.4] depending on the analyses.


Overview of data

These data files are derived from electroretinography (ERG) recordings conducted on individual nocturnal coral reef fish. Three species were assessed: Ostorhinchus compressus (referred to as cardinalfish in Dryad data files), Neoniphon sammara (squirrelfish) and Myripristis violacea (soldierfish). They were collected as described below. Further details of data collection can also be found in the associated preprint (https://www.biorxiv.org/content/10.1101/2022.11.27.518067v1). Eye diameter for each individual is also given in a separate file in this dataset (in millimetres).


Description of individual data files

Name: EyeDiameter_AllSpecies.tsv

Size: 250 bytes
Description of data: this file contains eye diameter (in millimetres) of each individual fish used in electroretinography recordings.

Species and replicates: Measurements were obtained for Ostorhinchus compressus (a cardinalfish; n = 10 individuals), Myripristis violacea (a soldierfish; n = 8 individuals) and Neoniphon sammara (a squirrelfish; n = 9 individuals).

Description of methods used to generate data: Eye diameter was measured in millimetres from photographs using the image processing software, Fiji.

Name: TemporalResolutionERG_AllSpecies.tsv

Size: 880 bytes
Description of data: this file contains results from temporal resolution experiments. Data are provided as maximal flicker fusion frequency (FFF) values in hertz (Hz).

Species and replicates: Measurements were obtained for Ostorhinchus compressus, Myripristis violacea and Neoniphon sammara (all species: n = 3 and 5 individuals each for day and night recordings, respectively, for both dim and bright stimuli).

Description of methods used to generate data: Corneal ERG recordings were conducted in vivo on whole, intact eyes to assess visual function. Fish were acclimatised to the recording chamber for 30 min, anaesthetised with 0.2 mL clove oil/litre seawater, immobilised with an intramuscular injection of 8.5 mg/kg gallamine triethiodide and ventilated with oxygenated seawater. After ≥40 min of dark adaptation, light stimuli were delivered to the eye using a custom-built, calibrated, broad-spectrum light source controlled via a PowerLab 4/26 DAQ module. Visual responses were detected through silver wire electrodes placed on the surface of the eye, amplified via a DP-103 amplifier and acquired in LabChart 8 (v8.1.16). The system was grounded to the water of the recording chamber. Recordings were conducted at 28 ± 1˚C at both day and night to control for any effects of temperature and circadian rhythm, respectively. Recordings were performed at the Lizard Island Research Station (LIRS) or the Queensland Brain Institute (QBI).
The temporal resolution of vision was assessed using flicker fusion frequency (FFF) ERGs. FFF is the point at which evenly spaced light pulses can no longer be distinguished as separate. Dark-adapted FFF ERGs were recorded by increasing the frequency of white light stimuli of constant intensity from 5 Hz to 95 Hz at increments of 5 Hz. Light pulses were 10 ms in duration and were repeated 30 times. Recordings were conducted for bright (384 lux) and dim (4 lux) stimuli. The FFF threshold was determined either through visual inspection (at lower frequencies, <65 Hz) or by using the power spectrum to differentiate the signal and noise (at higher frequencies, ≥65 Hz).

Name: LuminousSensitivityERGData_AllSpeciesCombined_Revised.csv

Size: 14 KB
Description of data: this file contains results from absolute sensitivity experiments. Data labelled as "Normalised to Vmax" are provided as a percentage of the maximal response recorded for each individual per stimulus intensity step (given in lux). Data labelled as "Eye size Normalised" are provided as the percentage of the maximal response divided by the eye diamter for each individual per stimulus intensity step.
Species and replicates: Measurements were obtained for Ostorhinchus compressus (n = 5 individuals each for day and night recordings, labelled as Fish 1, Fish 2, etc.), Myripristis violacea (n = 4 individuals each for day and night recordings) and Neoniphon sammara (n = 4 and 5 individuals for day and night recordings, respectively).

Description of methods used to generate data: Corneal ERG recordings were conducted in vivo on whole, intact eyes to assess visual function. Fish were acclimatised to the recording chamber for 30 min, anaesthetised with 0.2 mL clove oil/litre seawater, immobilised with an intramuscular injection of 8.5 mg/kg gallamine triethiodide and ventilated with oxygenated seawater. After ≥40 min of dark adaptation, light stimuli were delivered to the eye using a custom-built, calibrated, broad-spectrum light source controlled via a PowerLab 4/26 DAQ module. Visual responses were detected through silver wire electrodes placed on the surface of the eye, amplified via a DP-103 amplifier and acquired in LabChart 8 v8.1.16. The system was grounded to the water of the recording chamber. Recordings were conducted at 28 ± 1˚C at both day and night to control for any effects of temperature and circadian rhythm, respectively. Recordings were performed at the Lizard Island Research Station (LIRS) or the Queensland Brain Institute (QBI).

The absolute (luminous) sensitivity of vision was determined using V/logI curves, which plot the normalised amplitude of the response (V) against the log of the intensity (I). These ERGs were recorded by increasing the intensity of a white light from 2.4x10-8 to 240,000 lux [i.e., -7.6 to 5.4 log10(lux)] in 0.3-0.6 log unit steps. Light stimuli were 100 ms pulses presented at 0.1 – 0.4 Hz and were repeated ten times for each intensity. The mean response amplitudes were normalised to the maximal response (Vmax) and plotted against stimulus intensity to obtain the V/logI curve (labelled as "Normalised to Vmax" in Dryad data files). The area under the curve (AUC) was calculated as a proxy for the magnitude and breadth of the visual responses. AUC was calculated for either all intensities, dim intensities (<0.002 lux) or bright intensities (>10 lux) for each species. To isolate the effect of the multibank retina, the Vmax-normalised responses were also normalised to eye size (to obtain responses per unit of retina) and analysed again as described above (labelled as "Eye Size Normalised" in Dryad data files).

Name: LuminousSensitivityERGData_CardinalfishLocationComparison_Revised.csv

Size: 2 KB
Description of data: Data are provided as a percentage of the maximal response recorded for each individual per stimulus intensity step (given in lux).
Species and replicates: Measurements were obtained from Ostorhinchus compressus in two recording locations: the Queensland Brain Insitute (QBI) in Brisbane, Australia (n = 5 individuals) and the Lizard Island Research Station (LIRS) on the northern Great Barrier Reef, Australia (n = 2 individuals). All recordings were conducted during the day.Description of methods used to generate data: These data were collected in the same way as described above for the file "LuminousSensitivityERG_AllSpecies.tsv". However, recordings were taken at both Lizard Island Research Station, Australia (field) and Queensland Brain Institute, Australia (lab) to compare results between the recording locations.


Explanation of Update on 2023.10.03

Originally the b wave amplitudes in the luminous sensitivity ERG files were calculated from the isoelectric line. During the peer review process, a reviewer pointed out that the b wave amplitude would be affected by a deepening of the a wave at higher light intensities. Thus, the reviewer suggested that it would be more correct to calculate the b wave amplitude from the base of the a wave instead of the isoelectric line. This suggestion was also consistent with previously published analysis approaches and so was applied to the dataset. This change in analysis approach is incorporated into the updated luminous sensitivity ERG files.

Methods

Data are derived from electroretinograms recorded from individual nocturnal coral reef fish as described in the associated preprint. 

Data are either normalised to the maximal response (Vmax) or to both the maximal response and eye size.

Eye diameter (in millimetres) is given in an additional file.

Usage notes

Files are given in tsv format. No proprietary software is required to open the files or manipulate the data.

Funding

Australian Research Council