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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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Intensity-response V/logI) functions and thresholds of the electroretinogram responses to 2 s stimuli. In A and B, the V/logI curves of the ON transients (left) and OFF transients (right) are presented, obtained in the wild-type flies (open symbols, dashed lines, n=10) and in the  mutant hclBT2 (filled symbols, solid lines, n=10) under dark adaptation (DA, black squares) as well as under three levels of background illumination (4.66 log quanta s−1 μm−2, blue circles; 5.66 log quanta s−1 μm−2, green triangles; 6.66 log quanta s−1 μm−2, orange diamonds). In A, the response amplitude in mV versus log stimulus intensity It) is represented. The amplitudes of both ON and OFF transients are increased in the hclBT2 mutant (two way analysis of variance [ANOVA], 10−14<p<0.01 for ON and OFF responses under different backgrounds), the effect of the mutation being more pronounced with respect to the ON responses. In B, the same functions are normalized to Vmax. The relative sensitivity of the ON transients, obtained in hclBT2 flies under dark adaptation as well as under the dimmest background, is decreased (the curves are shifted to the right, p<0.01), while no change in relative sensitivity is observed under the two brighter backgrounds. Thus, in the hclB mutant, the shift of the ON transient V/logI curve along the intensity axis during light adaptation occurs within a narrower stimulus intensity range. The ON transient V/logI curves in the light adapted mutant are steeper and the dynamic range is narrowed by about 1 log unit (two way ANOVA, p=0.0035). The relative sensitivity and the dynamic range of the OFF transients are not significantly changed. In C, the thresholds of the electroretinogram (ERG) ON (left) and OFF (right) transients are presented obtained under dark adaptation (DA), as well as under three levels of background illumination. The thresholds are estimated using 0.5 mV criterion amplitude. The thresholds of the wild-type flies, (gray columns) and the  mutant hclBT2 (pink columns) are compared. The thresholds of the hclBT2 mutant transients are significantly lower (two-way ANOVA, p=2.34×10−4 for ON responses; p=0.026 for OFF responses) indicating an increased absolute sensitivity of the mutant responses.
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f3: Intensity-response V/logI) functions and thresholds of the electroretinogram responses to 2 s stimuli. In A and B, the V/logI curves of the ON transients (left) and OFF transients (right) are presented, obtained in the wild-type flies (open symbols, dashed lines, n=10) and in the mutant hclBT2 (filled symbols, solid lines, n=10) under dark adaptation (DA, black squares) as well as under three levels of background illumination (4.66 log quanta s−1 μm−2, blue circles; 5.66 log quanta s−1 μm−2, green triangles; 6.66 log quanta s−1 μm−2, orange diamonds). In A, the response amplitude in mV versus log stimulus intensity It) is represented. The amplitudes of both ON and OFF transients are increased in the hclBT2 mutant (two way analysis of variance [ANOVA], 10−14<p<0.01 for ON and OFF responses under different backgrounds), the effect of the mutation being more pronounced with respect to the ON responses. In B, the same functions are normalized to Vmax. The relative sensitivity of the ON transients, obtained in hclBT2 flies under dark adaptation as well as under the dimmest background, is decreased (the curves are shifted to the right, p<0.01), while no change in relative sensitivity is observed under the two brighter backgrounds. Thus, in the hclB mutant, the shift of the ON transient V/logI curve along the intensity axis during light adaptation occurs within a narrower stimulus intensity range. The ON transient V/logI curves in the light adapted mutant are steeper and the dynamic range is narrowed by about 1 log unit (two way ANOVA, p=0.0035). The relative sensitivity and the dynamic range of the OFF transients are not significantly changed. In C, the thresholds of the electroretinogram (ERG) ON (left) and OFF (right) transients are presented obtained under dark adaptation (DA), as well as under three levels of background illumination. The thresholds are estimated using 0.5 mV criterion amplitude. The thresholds of the wild-type flies, (gray columns) and the mutant hclBT2 (pink columns) are compared. The thresholds of the hclBT2 mutant transients are significantly lower (two-way ANOVA, p=2.34×10−4 for ON responses; p=0.026 for OFF responses) indicating an increased absolute sensitivity of the mutant responses.

Mentions: When long (2 s ON/ 8 s OFF) light stimuli were used, the ON transient increase in the hclB mutants was stimulus intensity–dependent under dark adaptation, as well as under the dimmest background used (p=1.57×10−4 and p=0.0034 for the two groups, respectively, n=10 for all groups of flies). In these conditions, the amplitude difference between the ON transients of the mutant and wild-type flies was more pronounced in responses to bright stimuli. The amplitudes of these responses in the hclB mutants approximated 200%–250% of the corresponding amplitudes in the wild-type controls (Figure 1B, Figure 3A). However, no interaction was found between the ON transient amplitude increase and the test stimulus intensity under the two brighter backgrounds. As a result, the absolute sensitivity of the mutant ON transients was increased (their thresholds were decreased, two way ANOVA, p=2.34×10−4, Figure 3C) in all conditions of ambient illumination, while the relative sensitivity of the ON transients was decreased (the V/logI curves were shifted to the right, p<0.01) under dark adaptation and under the lowest background, being unchanged under the two brighter backgrounds (Figure 3B). Thus, the adaptational shift of the ON transient V/logI curve occurred within a narrower intensity range in the mutant flies. The ON transient V/logI curves in the light-adapted mutants were steeper and the dynamic range of these responses was narrowed by about 1 log unit (two way ANOVA, p=0.0035; Figure 3B). Similar to the responses to 0.3 s stimuli, the amplitudes of the OFF transients of the hclB mutants approximated 120% of the amplitudes of the corresponding responses in the wild-type flies (two way ANOVA, p=7.11×10−7, Figure 3A). The absolute sensitivity of the mutant OFF responses was increased (two way ANOVA, p=0.026 for the decrease of their thresholds; Figure 3C), while the relative sensitivity of these responses was not significantly changed (Figure 3B). The small narrowing of the response dynamic range of the OFF transients was also not significant.


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)

Intensity-response V/logI) functions and thresholds of the electroretinogram responses to 2 s stimuli. In A and B, the V/logI curves of the ON transients (left) and OFF transients (right) are presented, obtained in the wild-type flies (open symbols, dashed lines, n=10) and in the  mutant hclBT2 (filled symbols, solid lines, n=10) under dark adaptation (DA, black squares) as well as under three levels of background illumination (4.66 log quanta s−1 μm−2, blue circles; 5.66 log quanta s−1 μm−2, green triangles; 6.66 log quanta s−1 μm−2, orange diamonds). In A, the response amplitude in mV versus log stimulus intensity It) is represented. The amplitudes of both ON and OFF transients are increased in the hclBT2 mutant (two way analysis of variance [ANOVA], 10−14<p<0.01 for ON and OFF responses under different backgrounds), the effect of the mutation being more pronounced with respect to the ON responses. In B, the same functions are normalized to Vmax. The relative sensitivity of the ON transients, obtained in hclBT2 flies under dark adaptation as well as under the dimmest background, is decreased (the curves are shifted to the right, p<0.01), while no change in relative sensitivity is observed under the two brighter backgrounds. Thus, in the hclB mutant, the shift of the ON transient V/logI curve along the intensity axis during light adaptation occurs within a narrower stimulus intensity range. The ON transient V/logI curves in the light adapted mutant are steeper and the dynamic range is narrowed by about 1 log unit (two way ANOVA, p=0.0035). The relative sensitivity and the dynamic range of the OFF transients are not significantly changed. In C, the thresholds of the electroretinogram (ERG) ON (left) and OFF (right) transients are presented obtained under dark adaptation (DA), as well as under three levels of background illumination. The thresholds are estimated using 0.5 mV criterion amplitude. The thresholds of the wild-type flies, (gray columns) and the  mutant hclBT2 (pink columns) are compared. The thresholds of the hclBT2 mutant transients are significantly lower (two-way ANOVA, p=2.34×10−4 for ON responses; p=0.026 for OFF responses) indicating an increased absolute sensitivity of the mutant responses.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f3: Intensity-response V/logI) functions and thresholds of the electroretinogram responses to 2 s stimuli. In A and B, the V/logI curves of the ON transients (left) and OFF transients (right) are presented, obtained in the wild-type flies (open symbols, dashed lines, n=10) and in the mutant hclBT2 (filled symbols, solid lines, n=10) under dark adaptation (DA, black squares) as well as under three levels of background illumination (4.66 log quanta s−1 μm−2, blue circles; 5.66 log quanta s−1 μm−2, green triangles; 6.66 log quanta s−1 μm−2, orange diamonds). In A, the response amplitude in mV versus log stimulus intensity It) is represented. The amplitudes of both ON and OFF transients are increased in the hclBT2 mutant (two way analysis of variance [ANOVA], 10−14<p<0.01 for ON and OFF responses under different backgrounds), the effect of the mutation being more pronounced with respect to the ON responses. In B, the same functions are normalized to Vmax. The relative sensitivity of the ON transients, obtained in hclBT2 flies under dark adaptation as well as under the dimmest background, is decreased (the curves are shifted to the right, p<0.01), while no change in relative sensitivity is observed under the two brighter backgrounds. Thus, in the hclB mutant, the shift of the ON transient V/logI curve along the intensity axis during light adaptation occurs within a narrower stimulus intensity range. The ON transient V/logI curves in the light adapted mutant are steeper and the dynamic range is narrowed by about 1 log unit (two way ANOVA, p=0.0035). The relative sensitivity and the dynamic range of the OFF transients are not significantly changed. In C, the thresholds of the electroretinogram (ERG) ON (left) and OFF (right) transients are presented obtained under dark adaptation (DA), as well as under three levels of background illumination. The thresholds are estimated using 0.5 mV criterion amplitude. The thresholds of the wild-type flies, (gray columns) and the mutant hclBT2 (pink columns) are compared. The thresholds of the hclBT2 mutant transients are significantly lower (two-way ANOVA, p=2.34×10−4 for ON responses; p=0.026 for OFF responses) indicating an increased absolute sensitivity of the mutant responses.
Mentions: When long (2 s ON/ 8 s OFF) light stimuli were used, the ON transient increase in the hclB mutants was stimulus intensity–dependent under dark adaptation, as well as under the dimmest background used (p=1.57×10−4 and p=0.0034 for the two groups, respectively, n=10 for all groups of flies). In these conditions, the amplitude difference between the ON transients of the mutant and wild-type flies was more pronounced in responses to bright stimuli. The amplitudes of these responses in the hclB mutants approximated 200%–250% of the corresponding amplitudes in the wild-type controls (Figure 1B, Figure 3A). However, no interaction was found between the ON transient amplitude increase and the test stimulus intensity under the two brighter backgrounds. As a result, the absolute sensitivity of the mutant ON transients was increased (their thresholds were decreased, two way ANOVA, p=2.34×10−4, Figure 3C) in all conditions of ambient illumination, while the relative sensitivity of the ON transients was decreased (the V/logI curves were shifted to the right, p<0.01) under dark adaptation and under the lowest background, being unchanged under the two brighter backgrounds (Figure 3B). Thus, the adaptational shift of the ON transient V/logI curve occurred within a narrower intensity range in the mutant flies. The ON transient V/logI curves in the light-adapted mutants were steeper and the dynamic range of these responses was narrowed by about 1 log unit (two way ANOVA, p=0.0035; Figure 3B). Similar to the responses to 0.3 s stimuli, the amplitudes of the OFF transients of the hclB mutants approximated 120% of the amplitudes of the corresponding responses in the wild-type flies (two way ANOVA, p=7.11×10−7, Figure 3A). The absolute sensitivity of the mutant OFF responses was increased (two way ANOVA, p=0.026 for the decrease of their thresholds; Figure 3C), while the relative sensitivity of these responses was not significantly changed (Figure 3B). The small narrowing of the response dynamic range of the OFF transients was also not significant.

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