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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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Dynamics of dark sensitivity recovery after short-term light adaptation. A continuous series of 0.3 s stimuli was presented in the dark. Short-time light adaptation was achieved by using 2 s adapting stimuli (denoted by bars under the time scale). A: Dynamics of sensitivity recovery of the ON transient (left), ERG receptor component (in the middle) and OFF transient (right) in the wild-type flies (black squares; n=17), and hclBT2  mutant (red circles; n=15). Test stimulus intensity It)=4.73 log quanta s−1 μm−2; background intensity Ib)=6.66 log quanta s−1 μm−2. While instant sensitivity recovery of the ON and OFF transients is seen in wild-type flies, the sensitivity recovery in the hclBT2 mutants is delayed (two way analysis of variance [ANOVA], p=7.42.10−10 for the ON response and p=6.8.10−8 for the OFF response in these particular conditions). B: Postadaptational potentiation of the ON transient in the wild-type-flies (n=22) obtained using the following combination of test and adapting stimuli: It=4.73 log quanta s−1 μm−2, Ib=6.16 log quanta s−1 μm−2. Postadaptational potentiation is lacking in the hclBT2 (n=19) mutant flies. All labels are as in A. C: Original electroretinogram (ERG) records, obtained from a wild-type control fly (in the middle), hclBT2 mutant (on the left), and hclBT1 mutant (on the right). Stimulation conditions are as in B, In the first few seconds after the termination of the 2 s light-adapting stimulus, a postadaptational potentiation is seen in the wild-type fly, while a delayed sensitivity recovery is seen in the two mutants.
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f5: Dynamics of dark sensitivity recovery after short-term light adaptation. A continuous series of 0.3 s stimuli was presented in the dark. Short-time light adaptation was achieved by using 2 s adapting stimuli (denoted by bars under the time scale). A: Dynamics of sensitivity recovery of the ON transient (left), ERG receptor component (in the middle) and OFF transient (right) in the wild-type flies (black squares; n=17), and hclBT2 mutant (red circles; n=15). Test stimulus intensity It)=4.73 log quanta s−1 μm−2; background intensity Ib)=6.66 log quanta s−1 μm−2. While instant sensitivity recovery of the ON and OFF transients is seen in wild-type flies, the sensitivity recovery in the hclBT2 mutants is delayed (two way analysis of variance [ANOVA], p=7.42.10−10 for the ON response and p=6.8.10−8 for the OFF response in these particular conditions). B: Postadaptational potentiation of the ON transient in the wild-type-flies (n=22) obtained using the following combination of test and adapting stimuli: It=4.73 log quanta s−1 μm−2, Ib=6.16 log quanta s−1 μm−2. Postadaptational potentiation is lacking in the hclBT2 (n=19) mutant flies. All labels are as in A. C: Original electroretinogram (ERG) records, obtained from a wild-type control fly (in the middle), hclBT2 mutant (on the left), and hclBT1 mutant (on the right). Stimulation conditions are as in B, In the first few seconds after the termination of the 2 s light-adapting stimulus, a postadaptational potentiation is seen in the wild-type fly, while a delayed sensitivity recovery is seen in the two mutants.

Mentions: The time course of sensitivity recovery of the ERG responses after termination of light adapting stimuli with a few seconds’ duration was assessed by comparing the amplitudes of the ERG responses to 0.3 s stimuli in the periods, preceding and following presentation of adapting stimuli with 2 to 20 s duration and three intensities, specifically Ib1=5.66 log quanta s−1 μm−2, Ib2=6.16 log quanta s−1 μm−2, and Ib3=6.66 log quanta s−1 μm−2. The 0.3 s test stimulus duration was the shortest that allowed for reliable separation between the ON and OFF transients. The following two test stimulus intensities were used: 3.73 and 4.73 log quanta s−1 μm−2. The first was below the threshold of the ERG receptor component, so that the two ERG transients were recorded in isolation. The second elicited both the receptor component and transients, thus allowing for comparison of sensitivity changes of the receptor and LMC responses. The difference between the hclB mutants and the wild-type flies was best manifested when 2 s adapting stimuli were used. Depending on the particular combinations of test and adapting stimuli (the number [n] of the flies in the groups varied between 10 and 20), the following results were obtained: 1) In most cases, in the postadaptational period, the ON and OFF transients of the wild-type flies showed instant sensitivity recovery (Figure 5A). 2) The recovery took several seconds when the dimmer stimulus was combined with a very bright background (not shown). 3) When the brighter test stimulus was combined with Ib1 and Ib2, postadaptational potentiation was observed (Figure 5B,C). The ON transient amplitude increased up to 120% of the preadaptational value, on average, while only a few percent increase of the OFF transient amplitude was observed. The amplitude of the ERG receptor component was significantly diminished during the first few seconds of the postadaptational period in all conditions tested, so in wild-type flies, a clear discrepancy was observed between the dynamics of sensitivity changes of the receptor and postreceptoral ERG components. In the hclB mutants, the ON and OFF transient sensitivity recovery was significantly delayed in all conditions tested (two-way ANOVA, with the Bonferroni test, 10−15<p<10−4 for different combinations of test and adapting stimuli; Figure 5). Some small postadaptational potentiation was only occasionally seen. The dynamics of sensitivity recovery was similar between the receptor and postreceptoral ERG components.


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)

Dynamics of dark sensitivity recovery after short-term light adaptation. A continuous series of 0.3 s stimuli was presented in the dark. Short-time light adaptation was achieved by using 2 s adapting stimuli (denoted by bars under the time scale). A: Dynamics of sensitivity recovery of the ON transient (left), ERG receptor component (in the middle) and OFF transient (right) in the wild-type flies (black squares; n=17), and hclBT2  mutant (red circles; n=15). Test stimulus intensity It)=4.73 log quanta s−1 μm−2; background intensity Ib)=6.66 log quanta s−1 μm−2. While instant sensitivity recovery of the ON and OFF transients is seen in wild-type flies, the sensitivity recovery in the hclBT2 mutants is delayed (two way analysis of variance [ANOVA], p=7.42.10−10 for the ON response and p=6.8.10−8 for the OFF response in these particular conditions). B: Postadaptational potentiation of the ON transient in the wild-type-flies (n=22) obtained using the following combination of test and adapting stimuli: It=4.73 log quanta s−1 μm−2, Ib=6.16 log quanta s−1 μm−2. Postadaptational potentiation is lacking in the hclBT2 (n=19) mutant flies. All labels are as in A. C: Original electroretinogram (ERG) records, obtained from a wild-type control fly (in the middle), hclBT2 mutant (on the left), and hclBT1 mutant (on the right). Stimulation conditions are as in B, In the first few seconds after the termination of the 2 s light-adapting stimulus, a postadaptational potentiation is seen in the wild-type fly, while a delayed sensitivity recovery is seen in the two mutants.
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Related In: Results  -  Collection

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

f5: Dynamics of dark sensitivity recovery after short-term light adaptation. A continuous series of 0.3 s stimuli was presented in the dark. Short-time light adaptation was achieved by using 2 s adapting stimuli (denoted by bars under the time scale). A: Dynamics of sensitivity recovery of the ON transient (left), ERG receptor component (in the middle) and OFF transient (right) in the wild-type flies (black squares; n=17), and hclBT2 mutant (red circles; n=15). Test stimulus intensity It)=4.73 log quanta s−1 μm−2; background intensity Ib)=6.66 log quanta s−1 μm−2. While instant sensitivity recovery of the ON and OFF transients is seen in wild-type flies, the sensitivity recovery in the hclBT2 mutants is delayed (two way analysis of variance [ANOVA], p=7.42.10−10 for the ON response and p=6.8.10−8 for the OFF response in these particular conditions). B: Postadaptational potentiation of the ON transient in the wild-type-flies (n=22) obtained using the following combination of test and adapting stimuli: It=4.73 log quanta s−1 μm−2, Ib=6.16 log quanta s−1 μm−2. Postadaptational potentiation is lacking in the hclBT2 (n=19) mutant flies. All labels are as in A. C: Original electroretinogram (ERG) records, obtained from a wild-type control fly (in the middle), hclBT2 mutant (on the left), and hclBT1 mutant (on the right). Stimulation conditions are as in B, In the first few seconds after the termination of the 2 s light-adapting stimulus, a postadaptational potentiation is seen in the wild-type fly, while a delayed sensitivity recovery is seen in the two mutants.
Mentions: The time course of sensitivity recovery of the ERG responses after termination of light adapting stimuli with a few seconds’ duration was assessed by comparing the amplitudes of the ERG responses to 0.3 s stimuli in the periods, preceding and following presentation of adapting stimuli with 2 to 20 s duration and three intensities, specifically Ib1=5.66 log quanta s−1 μm−2, Ib2=6.16 log quanta s−1 μm−2, and Ib3=6.66 log quanta s−1 μm−2. The 0.3 s test stimulus duration was the shortest that allowed for reliable separation between the ON and OFF transients. The following two test stimulus intensities were used: 3.73 and 4.73 log quanta s−1 μm−2. The first was below the threshold of the ERG receptor component, so that the two ERG transients were recorded in isolation. The second elicited both the receptor component and transients, thus allowing for comparison of sensitivity changes of the receptor and LMC responses. The difference between the hclB mutants and the wild-type flies was best manifested when 2 s adapting stimuli were used. Depending on the particular combinations of test and adapting stimuli (the number [n] of the flies in the groups varied between 10 and 20), the following results were obtained: 1) In most cases, in the postadaptational period, the ON and OFF transients of the wild-type flies showed instant sensitivity recovery (Figure 5A). 2) The recovery took several seconds when the dimmer stimulus was combined with a very bright background (not shown). 3) When the brighter test stimulus was combined with Ib1 and Ib2, postadaptational potentiation was observed (Figure 5B,C). The ON transient amplitude increased up to 120% of the preadaptational value, on average, while only a few percent increase of the OFF transient amplitude was observed. The amplitude of the ERG receptor component was significantly diminished during the first few seconds of the postadaptational period in all conditions tested, so in wild-type flies, a clear discrepancy was observed between the dynamics of sensitivity changes of the receptor and postreceptoral ERG components. In the hclB mutants, the ON and OFF transient sensitivity recovery was significantly delayed in all conditions tested (two-way ANOVA, with the Bonferroni test, 10−15<p<10−4 for different combinations of test and adapting stimuli; Figure 5). Some small postadaptational potentiation was only occasionally seen. The dynamics of sensitivity recovery was similar between the receptor and postreceptoral ERG components.

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