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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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Temporal characteristics of the electroretinogram responses. In A, the peak latencies of the electroretinogram (ERG) ON (left) and OFF (right) transients are presented, obtained with 2 s stimuli under dark adaptation (black squares) and under background illumination of 5.66 log quanta s−1 μm−2 (green triangles). The results obtained in wild-type flies (empty symbols, dashed lines) and in hclBT2 mutants (filled symbols, solid lines) are represented. In the inset, original curves of a wild-type (black) and hclBT2 mutant (red) ON response are superimposed. The beginning of the records corresponds to the stimulus onset. Stimulus intensity=6.73 log quanta s−1 μm−2. Peak latency is delayed in the hclBT2 mutant (two way analysis of variance [ANOVA], 10−9<p<0.05 for different stimulation conditions). The delay is small in the dark-adapted responses, being well pronounced under light adaptation. In B, the results of low-pass filtering of the ERG ON transients are presented, obtained using 2 s stimuli in a wild-type fly (black squares) and hclBT2 (red circles) mutant. The amplitudes are normalized to the amplitudes of the nonfiltered signals (raw signals recorded at a bandpass of 0–1000 Hz). Stimulus intensity=6.73 log quanta s−1 μm−2. On the left, the results obtained under dark adaptation (DA) are presented. On the right, the results obtained under a background of 6.66 log quanta s−1 μm−2 (light adaptation, LA) are presented. The amplitudes of the mutant responses are decreased to a lesser extent by low-pass filtering. The difference is greater under light adaptation. This is indicative of the slower kinetics of the hclB mutant responses and implies that HCLB receptors may contribute to the high-pass filtering of the visual signal during light adaptation.
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f4: Temporal characteristics of the electroretinogram responses. In A, the peak latencies of the electroretinogram (ERG) ON (left) and OFF (right) transients are presented, obtained with 2 s stimuli under dark adaptation (black squares) and under background illumination of 5.66 log quanta s−1 μm−2 (green triangles). The results obtained in wild-type flies (empty symbols, dashed lines) and in hclBT2 mutants (filled symbols, solid lines) are represented. In the inset, original curves of a wild-type (black) and hclBT2 mutant (red) ON response are superimposed. The beginning of the records corresponds to the stimulus onset. Stimulus intensity=6.73 log quanta s−1 μm−2. Peak latency is delayed in the hclBT2 mutant (two way analysis of variance [ANOVA], 10−9<p<0.05 for different stimulation conditions). The delay is small in the dark-adapted responses, being well pronounced under light adaptation. In B, the results of low-pass filtering of the ERG ON transients are presented, obtained using 2 s stimuli in a wild-type fly (black squares) and hclBT2 (red circles) mutant. The amplitudes are normalized to the amplitudes of the nonfiltered signals (raw signals recorded at a bandpass of 0–1000 Hz). Stimulus intensity=6.73 log quanta s−1 μm−2. On the left, the results obtained under dark adaptation (DA) are presented. On the right, the results obtained under a background of 6.66 log quanta s−1 μm−2 (light adaptation, LA) are presented. The amplitudes of the mutant responses are decreased to a lesser extent by low-pass filtering. The difference is greater under light adaptation. This is indicative of the slower kinetics of the hclB mutant responses and implies that HCLB receptors may contribute to the high-pass filtering of the visual signal during light adaptation.

Mentions: The temporal characteristics of the ERG transients were also changed in the two hclB mutants. The ON and OFF transients had slower time course (see Figure 1 and Figure 4A –inset). The peak latencies of the ON and OFF transients were longer in the mutant as compared to the wild-type flies (10−9<p<0.05 for different stimulation conditions, n=10 for all groups of flies in each of the light stimulation conditions; Figure 4A). The difference was small under dark adaptation. Under light adaptation, a well expressed difference was obtained in responses to 2 s stimuli. The changes in the temporal characteristics of the mutant ERG transients were also tested by offline filtering of the ERG records. When low-pass filtered, the responses of the mutant flies were not dramatically reduced, while those of the wild-type flies were strongly diminished (Figure 4B). Conversely, the mutant fly responses were more sensitive to high-pass filtering (result not shown). The difference between the mutant and wild-type flies was more pronounced under light adaptation (Figure 4B, right).


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)

Temporal characteristics of the electroretinogram responses. In A, the peak latencies of the electroretinogram (ERG) ON (left) and OFF (right) transients are presented, obtained with 2 s stimuli under dark adaptation (black squares) and under background illumination of 5.66 log quanta s−1 μm−2 (green triangles). The results obtained in wild-type flies (empty symbols, dashed lines) and in hclBT2 mutants (filled symbols, solid lines) are represented. In the inset, original curves of a wild-type (black) and hclBT2 mutant (red) ON response are superimposed. The beginning of the records corresponds to the stimulus onset. Stimulus intensity=6.73 log quanta s−1 μm−2. Peak latency is delayed in the hclBT2 mutant (two way analysis of variance [ANOVA], 10−9<p<0.05 for different stimulation conditions). The delay is small in the dark-adapted responses, being well pronounced under light adaptation. In B, the results of low-pass filtering of the ERG ON transients are presented, obtained using 2 s stimuli in a wild-type fly (black squares) and hclBT2 (red circles) mutant. The amplitudes are normalized to the amplitudes of the nonfiltered signals (raw signals recorded at a bandpass of 0–1000 Hz). Stimulus intensity=6.73 log quanta s−1 μm−2. On the left, the results obtained under dark adaptation (DA) are presented. On the right, the results obtained under a background of 6.66 log quanta s−1 μm−2 (light adaptation, LA) are presented. The amplitudes of the mutant responses are decreased to a lesser extent by low-pass filtering. The difference is greater under light adaptation. This is indicative of the slower kinetics of the hclB mutant responses and implies that HCLB receptors may contribute to the high-pass filtering of the visual signal during light adaptation.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f4: Temporal characteristics of the electroretinogram responses. In A, the peak latencies of the electroretinogram (ERG) ON (left) and OFF (right) transients are presented, obtained with 2 s stimuli under dark adaptation (black squares) and under background illumination of 5.66 log quanta s−1 μm−2 (green triangles). The results obtained in wild-type flies (empty symbols, dashed lines) and in hclBT2 mutants (filled symbols, solid lines) are represented. In the inset, original curves of a wild-type (black) and hclBT2 mutant (red) ON response are superimposed. The beginning of the records corresponds to the stimulus onset. Stimulus intensity=6.73 log quanta s−1 μm−2. Peak latency is delayed in the hclBT2 mutant (two way analysis of variance [ANOVA], 10−9<p<0.05 for different stimulation conditions). The delay is small in the dark-adapted responses, being well pronounced under light adaptation. In B, the results of low-pass filtering of the ERG ON transients are presented, obtained using 2 s stimuli in a wild-type fly (black squares) and hclBT2 (red circles) mutant. The amplitudes are normalized to the amplitudes of the nonfiltered signals (raw signals recorded at a bandpass of 0–1000 Hz). Stimulus intensity=6.73 log quanta s−1 μm−2. On the left, the results obtained under dark adaptation (DA) are presented. On the right, the results obtained under a background of 6.66 log quanta s−1 μm−2 (light adaptation, LA) are presented. The amplitudes of the mutant responses are decreased to a lesser extent by low-pass filtering. The difference is greater under light adaptation. This is indicative of the slower kinetics of the hclB mutant responses and implies that HCLB receptors may contribute to the high-pass filtering of the visual signal during light adaptation.
Mentions: The temporal characteristics of the ERG transients were also changed in the two hclB mutants. The ON and OFF transients had slower time course (see Figure 1 and Figure 4A –inset). The peak latencies of the ON and OFF transients were longer in the mutant as compared to the wild-type flies (10−9<p<0.05 for different stimulation conditions, n=10 for all groups of flies in each of the light stimulation conditions; Figure 4A). The difference was small under dark adaptation. Under light adaptation, a well expressed difference was obtained in responses to 2 s stimuli. The changes in the temporal characteristics of the mutant ERG transients were also tested by offline filtering of the ERG records. When low-pass filtered, the responses of the mutant flies were not dramatically reduced, while those of the wild-type flies were strongly diminished (Figure 4B). Conversely, the mutant fly responses were more sensitive to high-pass filtering (result not shown). The difference between the mutant and wild-type flies was more pronounced under light adaptation (Figure 4B, right).

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