Robustness of Neural Coding inDrosophilaPhotoreceptors in the Absence of Slow Delayed Rectifier K+Channels

Vähäsöyrinki, Mikko; Niven, Jeremy E.; Hardie, Roger C.; Weckström, Matti; Juusola, Mikko

doi:10.1523/jneurosci.3316-05.2006

Cited by 61 publications

(103 citation statements)

References 51 publications

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“…The decreased input resistance in dSK Ϫ photoreceptors is similar to that found in Shaker and Shab mutant photoreceptors (Niven et al, 2003;Vähäsöyrinki et al, 2006), where it has been argued to compensate for mutant defects and underlie the robustness of encoding. In Shaker photoreceptors, the decrease in input resistance partially restores the efficient use of the operating voltage range (Niven et al, 2003).…”

Section: Robustness Of Dynamic Coding In Dsksupporting

confidence: 56%

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TheDrosophilaSK Channel (dSK) Contributes to Photoreceptor Performance by Mediating Sensitivity Control at the First Visual Network

Tayoun

Li²,

Chu³

et al. 2011

J. Neurosci.

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The contribution of the SK (small-conductance calcium-activated potassium) channel to neuronal functions in complex circuits underlying sensory processing and behavior is largely unknown in the absence of suitable animal models. Here, we generated a Drosophila line that lacks the single highly conserved SK gene in its genome (dSK). In R1-R6 photoreceptors, dSK encodes a slow Ca 2ϩ -activated K ϩ current similar to its mammalian counterparts. Compared with wild-type, dSK Ϫ photoreceptors and interneurons showed accelerated oscillatory responses and adaptation. These enhanced kinetics were accompanied with more depolarized dSK Ϫ photoreceptors axons, assigning a role for dSK in network gain control during light-to-dark transitions. However, compensatory network adaptation, through increasing activity between synaptic neighbors, overcame many detriments of missing dSK current enabling dSK Ϫ photoreceptors to maintain normal information transfer rates to naturalistic stimuli. While demonstrating important functional roles for dSK channel in the visual circuitry, these results also clarify how homeostatically balanced network functions can compensate missing or faulty ion channels.

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Section: Robustness Of Dynamic Coding In Dsksupporting

confidence: 56%

“…8G). These results highlight the inherit robustness of encoding in the lamina network (Niven et al, 2003;Vähäsöyrinki et al, 2006;Zheng et al, 2006).…”

Section: Back Bump Waveforms In Dskmentioning

confidence: 62%

TheDrosophilaSK Channel (dSK) Contributes to Photoreceptor Performance by Mediating Sensitivity Control at the First Visual Network

Tayoun

Li²,

Chu³

et al. 2011

J. Neurosci.

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“…Such precision would be impossible with today's optical imaging techniques, which are noisier and slower. Moreover, the method can be used to characterize small cells' electrical membrane properties both in current-and voltage-clamp configurations 5,29,33,36,[40][41][42]49 , providing valuable data for biophysical and empirical modeling approaches 7,8,11,33,[49][50][51][52][53][54] that link experiments to theory.…”

Section: Discussionmentioning

confidence: 99%

Electrophysiological Method for Recording Intracellular Voltage Responses of Drosophila Photoreceptors and Interneurons to Light Stimuli In Vivo

Juusola

Dau

Zheng

et al. 2016

JoVE

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Voltage responses of insect photoreceptors and visual interneurons can be accurately recorded with conventional sharp microelectrodes. The method described here enables the investigator to measure long-lasting (from minutes to hours) high-quality intracellular responses from single Drosophila R1-R6 photoreceptors and Large Monopolar Cells (LMCs) to light stimuli. Because the recording system has low noise, it can be used to study variability among individual cells in the fly eye, and how their outputs reflect the physical properties of the visual environment. We outline all key steps in performing this technique. The basic steps in constructing an appropriate electrophysiology set-up for recording, such as design and selection of the experimental equipment are described. We also explain how to prepare for recording by making appropriate (sharp) recording and (blunt) reference electrodes. Details are given on how to fix an intact fly in a bespoke fly-holder, prepare a small window in its eye and insert a recording electrode through this hole with minimal damage. We explain how to localize the center of a cell's receptive field, dark-or light-adapt the studied cell, and to record its voltage responses to dynamic light stimuli. Finally, we describe the criteria for stable normal recordings, show characteristic high-quality voltage responses of individual cells to different light stimuli, and briefly define how to quantify their signaling performance. Many aspects of the method are technically challenging and require practice and patience to master. But once learned and optimized for the investigator's experimental objectives, it grants outstanding in vivo neurophysiological data.

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“…Homeostatic plasticity may lead to altered signaling costs, as shown by robustness in neuronal signaling in the face of the loss of a delayed rectifier potassium channel in Drosophila photoreceptors (Vahasoyrinki et al, 2006). Because the cost of propagating action potentials is generally greater than the cost of synaptic transmission (Laughlin et al, 1998), the DCMDFETi pathway is likely to require less energy in solitarious locusts.…”

Section: Discussionmentioning

confidence: 99%

Compensatory Plasticity at an Identified Synapse Tunes a Visuomotor Pathway

Rogers¹,

Krapp²,

Burrows³

et al. 2007

J. Neurosci.

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We characterized homeostatic plasticity at an identified sensory-motor synapse in an insect, which maintains constant levels of motor drive as locusts transform from their solitarious phase to their gregarious swarming phase. The same mechanism produces behaviorally relevant changes in response timing that can be understood in the context of an animal's altered behavioral state. For individual animals of either phase, different looming objects elicited different spiking responses in a visual looming detector interneuron, descending contralateral movement detector (DCMD), yet its synaptic drive to a leg motoneuron, fast extensor tibiae (FETi), always had the same maximum amplitude. Gregarious locust DCMDs produced more action potentials and had higher firing frequencies, but individual postsynaptic potentials (PSPs) elicited in FETi were half the amplitude of those in solitarious locusts. A model suggested that this alone could not explain the similarity in overall amplitude, and we show that facilitation increased the maximum compound PSP amplitude in gregarious animals. There was the same linear relationship between times of peak DCMD firing before collision and the size/velocity of looming objects in both phases. The DCMD-FETi synapse transformed this relationship nonlinearly, such that peak amplitudes of compound PSPs occurred disproportionately earlier for smaller/faster objects. Furthermore, the peak PSP amplitude occurred earlier in gregarious than in solitarious locusts, indicating a differential tuning. Homeostatic modulation of the amplitude, together with a nonlinear synaptic transformation of timing, acted together to tune the DCMD-FETi system so that swarming gregarious locusts respond earlier to small moving objects, such as conspecifics, than solitarious locusts.

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Robustness of Neural Coding inDrosophilaPhotoreceptors in the Absence of Slow Delayed Rectifier K⁺Channels

Cited by 61 publications

References 51 publications

TheDrosophilaSK Channel (dSK) Contributes to Photoreceptor Performance by Mediating Sensitivity Control at the First Visual Network

TheDrosophilaSK Channel (dSK) Contributes to Photoreceptor Performance by Mediating Sensitivity Control at the First Visual Network

Electrophysiological Method for Recording Intracellular Voltage Responses of <em>Drosophila</em> Photoreceptors and Interneurons to Light Stimuli <em>In Vivo</em>

Compensatory Plasticity at an Identified Synapse Tunes a Visuomotor Pathway

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