Evidence for dynamic network regulation of Drosophila photoreceptor function from mutants lacking the neurotransmitter histamine
Synaptic feedback from interneurons to photoreceptors can help to optimize visual information flow by balancing its allocation on retinal pathways under changing light conditions. But little is known about how this critical network operation is regulated dynamically. Here, we investigate this questi...
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doaj-131d5de0bbbe4eb38f66bc9a1c08763d2020-11-25T00:07:13ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102016-03-011010.3389/fncir.2016.00019186191Evidence for dynamic network regulation of Drosophila photoreceptor function from mutants lacking the neurotransmitter histamineAn eDau0Uwe eFriederich1Sidhartha eDongre2Xiaofeng eLi3Murali K. Bollepalli4Roger Clayton Hardie5Mikko eJuusola6Mikko eJuusola7University of SheffieldUniversity of SheffieldUniversity of SheffieldUniversity of SheffieldUniversity of CambridgeUniversity of CambridgeUniversity of SheffieldBeijing Normal UniversitySynaptic feedback from interneurons to photoreceptors can help to optimize visual information flow by balancing its allocation on retinal pathways under changing light conditions. But little is known about how this critical network operation is regulated dynamically. Here, we investigate this question by comparing signaling properties and performance of wild-type Drosophila R1-R6 photoreceptors to those of the hdcJK910 mutant, which lacks the neurotransmitter histamine and therefore cannot transmit information to interneurons. Recordings show that hdcJK910 photoreceptors sample similar amounts of information from naturalistic stimulation to wild-type photoreceptors, but this information is packaged in smaller responses, especially under bright illumination. Analyses reveal how these altered dynamics primarily resulted from network overload that affected hdcJK910 photoreceptors in two ways. First, the missing inhibitory histamine input to interneurons almost certainly depolarized them irrevocably, which in turn increased their excitatory feedback to hdcJK910 R1-R6s. This tonic excitation depolarized the photoreceptors to artificially high potentials, reducing their operational range. Second, rescuing histamine input to interneurons in hdcJK910 mutant also restored their normal phasic feedback modulation to R1-R6s, causing photoreceptor output to accentuate dynamic intensity differences at bright illumination, similar to the wild-type. These results provide mechanistic explanations of how synaptic feedback connections optimize information packaging in photoreceptor output and novel insight into the operation and design of dynamic network regulation of sensory neurons.http://journal.frontiersin.org/Journal/10.3389/fncir.2016.00019/fullHistaminePhotoreceptor Cells, InvertebrateVisual PerceptionInformation Theory and Signal Processingfeedback synapses |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
An eDau Uwe eFriederich Sidhartha eDongre Xiaofeng eLi Murali K. Bollepalli Roger Clayton Hardie Mikko eJuusola Mikko eJuusola |
spellingShingle |
An eDau Uwe eFriederich Sidhartha eDongre Xiaofeng eLi Murali K. Bollepalli Roger Clayton Hardie Mikko eJuusola Mikko eJuusola Evidence for dynamic network regulation of Drosophila photoreceptor function from mutants lacking the neurotransmitter histamine Frontiers in Neural Circuits Histamine Photoreceptor Cells, Invertebrate Visual Perception Information Theory and Signal Processing feedback synapses |
author_facet |
An eDau Uwe eFriederich Sidhartha eDongre Xiaofeng eLi Murali K. Bollepalli Roger Clayton Hardie Mikko eJuusola Mikko eJuusola |
author_sort |
An eDau |
title |
Evidence for dynamic network regulation of Drosophila photoreceptor function from mutants lacking the neurotransmitter histamine |
title_short |
Evidence for dynamic network regulation of Drosophila photoreceptor function from mutants lacking the neurotransmitter histamine |
title_full |
Evidence for dynamic network regulation of Drosophila photoreceptor function from mutants lacking the neurotransmitter histamine |
title_fullStr |
Evidence for dynamic network regulation of Drosophila photoreceptor function from mutants lacking the neurotransmitter histamine |
title_full_unstemmed |
Evidence for dynamic network regulation of Drosophila photoreceptor function from mutants lacking the neurotransmitter histamine |
title_sort |
evidence for dynamic network regulation of drosophila photoreceptor function from mutants lacking the neurotransmitter histamine |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Neural Circuits |
issn |
1662-5110 |
publishDate |
2016-03-01 |
description |
Synaptic feedback from interneurons to photoreceptors can help to optimize visual information flow by balancing its allocation on retinal pathways under changing light conditions. But little is known about how this critical network operation is regulated dynamically. Here, we investigate this question by comparing signaling properties and performance of wild-type Drosophila R1-R6 photoreceptors to those of the hdcJK910 mutant, which lacks the neurotransmitter histamine and therefore cannot transmit information to interneurons. Recordings show that hdcJK910 photoreceptors sample similar amounts of information from naturalistic stimulation to wild-type photoreceptors, but this information is packaged in smaller responses, especially under bright illumination. Analyses reveal how these altered dynamics primarily resulted from network overload that affected hdcJK910 photoreceptors in two ways. First, the missing inhibitory histamine input to interneurons almost certainly depolarized them irrevocably, which in turn increased their excitatory feedback to hdcJK910 R1-R6s. This tonic excitation depolarized the photoreceptors to artificially high potentials, reducing their operational range. Second, rescuing histamine input to interneurons in hdcJK910 mutant also restored their normal phasic feedback modulation to R1-R6s, causing photoreceptor output to accentuate dynamic intensity differences at bright illumination, similar to the wild-type. These results provide mechanistic explanations of how synaptic feedback connections optimize information packaging in photoreceptor output and novel insight into the operation and design of dynamic network regulation of sensory neurons. |
topic |
Histamine Photoreceptor Cells, Invertebrate Visual Perception Information Theory and Signal Processing feedback synapses |
url |
http://journal.frontiersin.org/Journal/10.3389/fncir.2016.00019/full |
work_keys_str_mv |
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