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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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Related in: MedlinePlus

Intensity-response V/logI) functions and thresholds of the electroretinogram responses to 0.3 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 amplitude of both ON and OFF transients is increased in the hclB mutant, the effect of the mutation being more pronounced with respect to ON responses (two way analysis of variance [ANOVA], 10−15<p<0.05 for ON and OFF responses under different backgrounds). In B, the same functions are normalized to Vmax. The relative sensitivity of the ON and OFF transients, assessed by the I50 points of the V/log I curves, is mostly not significantly different between the wild-type and hclB mutant flies. The steepness of the V/log I curves of the ON transients is higher in the hclB mutant and thus the ON-response dynamic range is narrowed (two way ANOVA, p=0.015). 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=1.22×10−5 for ON responses; p=0.032 for OFF responses), indicating an increased absolute sensitivity of the mutant responses.
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f2: Intensity-response V/logI) functions and thresholds of the electroretinogram responses to 0.3 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 amplitude of both ON and OFF transients is increased in the hclB mutant, the effect of the mutation being more pronounced with respect to ON responses (two way analysis of variance [ANOVA], 10−15<p<0.05 for ON and OFF responses under different backgrounds). In B, the same functions are normalized to Vmax. The relative sensitivity of the ON and OFF transients, assessed by the I50 points of the V/log I curves, is mostly not significantly different between the wild-type and hclB mutant flies. The steepness of the V/log I curves of the ON transients is higher in the hclB mutant and thus the ON-response dynamic range is narrowed (two way ANOVA, p=0.015). 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=1.22×10−5 for ON responses; p=0.032 for OFF responses), indicating an increased absolute sensitivity of the mutant responses.

Mentions: When short (0.3 s ON/ 1.2 s OFF) light stimuli were used, the amplitudes of the ON and OFF transients of the hclB mutants were increased under both dark and light adaptation (Figure 1A, Figure 2A). The ON transient increase was greater and approximated 150%–170% of the amplitude obtained in wild-type flies. The OFF transient increase did not exceed 120%. No significant interaction was found with stimulus intensity. Therefore, the absolute sensitivity of the mutant transients was increased, as indicated by their lower thresholds (two-way ANOVA, p=1.22×10−5 for ON responses and p=0.032 for OFF responses, n=10 for all groups of flies; Figure 2C), while the relative sensitivity of the transients (assessed by the σ [I50] value) was not significantly changed (Figure 2 B). With increasing background intensity and V/logI function steepness, the OFF response threshold diminution became less pronounced (insignificant under the brighter backgrounds). The V/log I curves of the mutant ON transients were slightly steeper than the corresponding curves of the wild-type flies (n value in the Naka-Rushton equation was greater, two way ANOVA, p=0.015) and the dynamic range of the ON transients was thus narrowed by about 0.5 log units.


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 0.3 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 amplitude of both ON and OFF transients is increased in the hclB mutant, the effect of the mutation being more pronounced with respect to ON responses (two way analysis of variance [ANOVA], 10−15<p<0.05 for ON and OFF responses under different backgrounds). In B, the same functions are normalized to Vmax. The relative sensitivity of the ON and OFF transients, assessed by the I50 points of the V/log I curves, is mostly not significantly different between the wild-type and hclB mutant flies. The steepness of the V/log I curves of the ON transients is higher in the hclB mutant and thus the ON-response dynamic range is narrowed (two way ANOVA, p=0.015). 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=1.22×10−5 for ON responses; p=0.032 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

f2: Intensity-response V/logI) functions and thresholds of the electroretinogram responses to 0.3 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 amplitude of both ON and OFF transients is increased in the hclB mutant, the effect of the mutation being more pronounced with respect to ON responses (two way analysis of variance [ANOVA], 10−15<p<0.05 for ON and OFF responses under different backgrounds). In B, the same functions are normalized to Vmax. The relative sensitivity of the ON and OFF transients, assessed by the I50 points of the V/log I curves, is mostly not significantly different between the wild-type and hclB mutant flies. The steepness of the V/log I curves of the ON transients is higher in the hclB mutant and thus the ON-response dynamic range is narrowed (two way ANOVA, p=0.015). 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=1.22×10−5 for ON responses; p=0.032 for OFF responses), indicating an increased absolute sensitivity of the mutant responses.
Mentions: When short (0.3 s ON/ 1.2 s OFF) light stimuli were used, the amplitudes of the ON and OFF transients of the hclB mutants were increased under both dark and light adaptation (Figure 1A, Figure 2A). The ON transient increase was greater and approximated 150%–170% of the amplitude obtained in wild-type flies. The OFF transient increase did not exceed 120%. No significant interaction was found with stimulus intensity. Therefore, the absolute sensitivity of the mutant transients was increased, as indicated by their lower thresholds (two-way ANOVA, p=1.22×10−5 for ON responses and p=0.032 for OFF responses, n=10 for all groups of flies; Figure 2C), while the relative sensitivity of the transients (assessed by the σ [I50] value) was not significantly changed (Figure 2 B). With increasing background intensity and V/logI function steepness, the OFF response threshold diminution became less pronounced (insignificant under the brighter backgrounds). The V/log I curves of the mutant ON transients were slightly steeper than the corresponding curves of the wild-type flies (n value in the Naka-Rushton equation was greater, two way ANOVA, p=0.015) and the dynamic range of the ON transients was thus narrowed by about 0.5 log units.

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