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Participation of the histamine receptor encoded by the gene hclB (HCLB) in visual sensitivity control: an electroretinographic study in Drosophila melanogaster.

Kupenova P, Yusein-Myashkova S - Mol. Vis. (2012)

Bottom Line: The slower kinetics of the ERG transients was also indicated by their lower sensitivity to low-pass filtering, the effect being more pronounced under light adaptation.In the hclB mutants the dark sensitivity recovery in similar conditions was significantly delayed.They modulate the temporal characteristics of visual responses in a way that improves the temporal resolution of the visual system and reduces redundant (low-frequency) information.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Medical University, Sofia, Bulgaria. pkupenova@abv.bg

ABSTRACT

Purpose: Histaminergic transmission in the first synapse of the visual system in Drosophila melanogaster is mediated by two types of histamine receptors: 1) encoded by the gene hclA (HCLA), which is expressed in the second-order neurons-the large monopolar cells of the lamina, and is absolutely required for forward signal transmission; and 2) encoded by the gene hclB (HCLB), which is expressed in epithelial glia, and is involved in modulation of synaptic transmission from photoreceptors to large monopolar cells. The aim of our study was to establish whether the HCLB receptor-mediated modulation of synaptic transmission 1) contributes to the process of light adaptation, and 2) is involved in the control of the dynamics of sensitivity recovery after short-term light adaptation.

Methods: The effects of mutations in the gene hclB, encoding the subunits of the histamine receptor HCLB, were studied on 1) the intensity-response (V/logI) function of electroretinographic (ERG) responses under dark adaptation, as well as under three levels of background illumination; and 2) the dynamics of the dark sensitivity recovery after short-term light adaptation.

Results: The amplitude of the photoreceptor component in the electroretinogram (ERG) was not significantly different between the hclB mutants and the wild-type flies, while the amplitude of the ERG ON and OFF transients, representing the activity of the second-order visual cells, was increased in the hclB mutants under both dark and light adaptation. The ON responses were affected to a greater degree. Under a given background, the ON response V/logI function was steeper and the response dynamic range was narrowed. The absolute sensitivity of the two transients was increased, as revealed by the decrease of their thresholds. The relative sensitivity of the transients, assessed by the semisaturation points of their V/logI functions, was decreased in ON responses to long (2 s) stimuli under dark and moderate light adaptation, being unchanged under bright backgrounds. Thus, the shift of the ON response V/logI function along the stimulus intensity axis during light adaptation occurred within a narrower range. The peak latencies of the ERG transients were delayed. The slower kinetics of the ERG transients was also indicated by their lower sensitivity to low-pass filtering, the effect being more pronounced under light adaptation. In wild-type flies, an instant dark sensitivity recovery or postadaptational potentiation of the ERG transients was usually observed after short-term light adaptation. In the hclB mutants the dark sensitivity recovery in similar conditions was significantly delayed.

Conclusions: The glial histamine receptor HCLB participates in visual sensitivity control at the level of the first synapse of the Drosophila visual system under a wide range of ambient illumination conditions and contributes to the process of light adaptation. The HCLB receptor-mediated modulation of synaptic gain helps avoid response saturation and increases the range of stimulus intensities within which dynamic responses can be generated. The HCLB receptors also speed up the sensitivity recovery after short-term light adaptation and contribute to the mechanism of postadaptational potentiation. They modulate the temporal characteristics of visual responses in a way that improves the temporal resolution of the visual system and reduces redundant (low-frequency) information.

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Individual electroretinogram records obtained under different light stimulation conditions from a wild-type fly -OR/Df(3R)E79, denoted as control and two hclB mutants—hclBT2/Df(3R)E79, a  mutant, and hclBT1/Df(3R)E79, denoted as hclBT2 and hclBT1, respectively. In A and B, electroretinogram (ERG) responses to 0.3 s and 2 s stimuli are represented, respectively. The numbers on the left denote test stimulus intensities (in log quanta s−1 μm−2). Responses obtained under dark adaptation (left) and light adaptation with a background of 4.66 log quanta s−1 μm−2 intensity (right) are represented. It is seen that the receptor component of the ERG has similar amplitude in both wild-type and mutant flies, while the ON and OFF transients’ amplitudes are significantly greater in the hclB mutants. It can also be observed that the overall duration of the transients is increased in the mutant flies.
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f1: Individual electroretinogram records obtained under different light stimulation conditions from a wild-type fly -OR/Df(3R)E79, denoted as control and two hclB mutants—hclBT2/Df(3R)E79, a mutant, and hclBT1/Df(3R)E79, denoted as hclBT2 and hclBT1, respectively. In A and B, electroretinogram (ERG) responses to 0.3 s and 2 s stimuli are represented, respectively. The numbers on the left denote test stimulus intensities (in log quanta s−1 μm−2). Responses obtained under dark adaptation (left) and light adaptation with a background of 4.66 log quanta s−1 μm−2 intensity (right) are represented. It is seen that the receptor component of the ERG has similar amplitude in both wild-type and mutant flies, while the ON and OFF transients’ amplitudes are significantly greater in the hclB mutants. It can also be observed that the overall duration of the transients is increased in the mutant flies.

Mentions: The ERGs of the two hclB mutants (hclBT2 and hclBT1) were similar to those of the wild-type flies in that they also consisted of a graded negative (receptor) component and two transient ones—a positive ON and a negative OFF transient, representing, as mentioned above, the activity of the LMCs in the lamina (Figure 1). However, while the amplitude of the receptor component was indistinguishable between the mutant flies and the wild-type controls, the amplitudes of the ERG transients were greater in the two mutants as compared to the wild-type flies (two-way ANOVA with the Bonferroni test; 10−15<p<0.05 for ON and OFF responses under different backgrounds, n=10 for all groups of flies in each of the light stimulation conditions). The ERG changes were similar in the two hclB mutants. To avoid redundancy, the results for the mutant hclBT2 are mostly illustrated in the text.


Participation of the histamine receptor encoded by the gene hclB (HCLB) in visual sensitivity control: an electroretinographic study in Drosophila melanogaster.

Kupenova P, Yusein-Myashkova S - Mol. Vis. (2012)

Individual electroretinogram records obtained under different light stimulation conditions from a wild-type fly -OR/Df(3R)E79, denoted as control and two hclB mutants—hclBT2/Df(3R)E79, a  mutant, and hclBT1/Df(3R)E79, denoted as hclBT2 and hclBT1, respectively. In A and B, electroretinogram (ERG) responses to 0.3 s and 2 s stimuli are represented, respectively. The numbers on the left denote test stimulus intensities (in log quanta s−1 μm−2). Responses obtained under dark adaptation (left) and light adaptation with a background of 4.66 log quanta s−1 μm−2 intensity (right) are represented. It is seen that the receptor component of the ERG has similar amplitude in both wild-type and mutant flies, while the ON and OFF transients’ amplitudes are significantly greater in the hclB mutants. It can also be observed that the overall duration of the transients is increased in the mutant flies.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3472930&req=5

f1: Individual electroretinogram records obtained under different light stimulation conditions from a wild-type fly -OR/Df(3R)E79, denoted as control and two hclB mutants—hclBT2/Df(3R)E79, a mutant, and hclBT1/Df(3R)E79, denoted as hclBT2 and hclBT1, respectively. In A and B, electroretinogram (ERG) responses to 0.3 s and 2 s stimuli are represented, respectively. The numbers on the left denote test stimulus intensities (in log quanta s−1 μm−2). Responses obtained under dark adaptation (left) and light adaptation with a background of 4.66 log quanta s−1 μm−2 intensity (right) are represented. It is seen that the receptor component of the ERG has similar amplitude in both wild-type and mutant flies, while the ON and OFF transients’ amplitudes are significantly greater in the hclB mutants. It can also be observed that the overall duration of the transients is increased in the mutant flies.
Mentions: The ERGs of the two hclB mutants (hclBT2 and hclBT1) were similar to those of the wild-type flies in that they also consisted of a graded negative (receptor) component and two transient ones—a positive ON and a negative OFF transient, representing, as mentioned above, the activity of the LMCs in the lamina (Figure 1). However, while the amplitude of the receptor component was indistinguishable between the mutant flies and the wild-type controls, the amplitudes of the ERG transients were greater in the two mutants as compared to the wild-type flies (two-way ANOVA with the Bonferroni test; 10−15<p<0.05 for ON and OFF responses under different backgrounds, n=10 for all groups of flies in each of the light stimulation conditions). The ERG changes were similar in the two hclB mutants. To avoid redundancy, the results for the mutant hclBT2 are mostly illustrated in the text.

Bottom Line: The slower kinetics of the ERG transients was also indicated by their lower sensitivity to low-pass filtering, the effect being more pronounced under light adaptation.In the hclB mutants the dark sensitivity recovery in similar conditions was significantly delayed.They modulate the temporal characteristics of visual responses in a way that improves the temporal resolution of the visual system and reduces redundant (low-frequency) information.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Medical University, Sofia, Bulgaria. pkupenova@abv.bg

ABSTRACT

Purpose: Histaminergic transmission in the first synapse of the visual system in Drosophila melanogaster is mediated by two types of histamine receptors: 1) encoded by the gene hclA (HCLA), which is expressed in the second-order neurons-the large monopolar cells of the lamina, and is absolutely required for forward signal transmission; and 2) encoded by the gene hclB (HCLB), which is expressed in epithelial glia, and is involved in modulation of synaptic transmission from photoreceptors to large monopolar cells. The aim of our study was to establish whether the HCLB receptor-mediated modulation of synaptic transmission 1) contributes to the process of light adaptation, and 2) is involved in the control of the dynamics of sensitivity recovery after short-term light adaptation.

Methods: The effects of mutations in the gene hclB, encoding the subunits of the histamine receptor HCLB, were studied on 1) the intensity-response (V/logI) function of electroretinographic (ERG) responses under dark adaptation, as well as under three levels of background illumination; and 2) the dynamics of the dark sensitivity recovery after short-term light adaptation.

Results: The amplitude of the photoreceptor component in the electroretinogram (ERG) was not significantly different between the hclB mutants and the wild-type flies, while the amplitude of the ERG ON and OFF transients, representing the activity of the second-order visual cells, was increased in the hclB mutants under both dark and light adaptation. The ON responses were affected to a greater degree. Under a given background, the ON response V/logI function was steeper and the response dynamic range was narrowed. The absolute sensitivity of the two transients was increased, as revealed by the decrease of their thresholds. The relative sensitivity of the transients, assessed by the semisaturation points of their V/logI functions, was decreased in ON responses to long (2 s) stimuli under dark and moderate light adaptation, being unchanged under bright backgrounds. Thus, the shift of the ON response V/logI function along the stimulus intensity axis during light adaptation occurred within a narrower range. The peak latencies of the ERG transients were delayed. The slower kinetics of the ERG transients was also indicated by their lower sensitivity to low-pass filtering, the effect being more pronounced under light adaptation. In wild-type flies, an instant dark sensitivity recovery or postadaptational potentiation of the ERG transients was usually observed after short-term light adaptation. In the hclB mutants the dark sensitivity recovery in similar conditions was significantly delayed.

Conclusions: The glial histamine receptor HCLB participates in visual sensitivity control at the level of the first synapse of the Drosophila visual system under a wide range of ambient illumination conditions and contributes to the process of light adaptation. The HCLB receptor-mediated modulation of synaptic gain helps avoid response saturation and increases the range of stimulus intensities within which dynamic responses can be generated. The HCLB receptors also speed up the sensitivity recovery after short-term light adaptation and contribute to the mechanism of postadaptational potentiation. They modulate the temporal characteristics of visual responses in a way that improves the temporal resolution of the visual system and reduces redundant (low-frequency) information.

Show MeSH
Related in: MedlinePlus