Transduction and Adaptation Mechanisms in the Cilium or Microvilli of Photoreceptors and Olfactory Receptors From Insects to Humans

Abbas, Farrukh; Vinberg, Frans

doi:10.3389/fncel.2021.662453

Cited by 25 publications

(9 citation statements)

References 235 publications

(168 reference statements)

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“…A split into separate channels downstream of L3 is also beneficial when the need for different types of gain control is not symmetrical, that is when the post-photoreceptor gain correction is differentially required to increase and decrease luminance gain. For example, dark adaptation in photoreceptors involves slow recovery of bleached visual pigments, and thus takes much longer (up to an hour) than light adaptation (3, 41, 42). In this scenario, the post-photoreceptor gain control may play a more extensive role in dark adaptation at fast timescales than in light adaptation.…”

Section: Discussionmentioning

confidence: 99%

Multifaceted luminance gain control beyond photoreceptors inDrosophila

Ketkar

Shao

Gjorgjieva

et al. 2023

Preprint

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Animals navigating in natural environments must handle vast changes in their sensory input. Visual systems, for example, handle changes in luminance at many timescales, from slow changes across the day to rapid changes during active behavior. To maintain luminance-invariant perception, visual systems must adapt their sensitivity to changing luminance at different timescales. We demonstrate that luminance gain control in photoreceptors alone is insufficient to explain luminance invariance at both fast and slow timescales and reveal the algorithms that adjust gain past photoreceptors in the fly eye. We combined imaging and behavioral experiments with computational modeling to show that, downstream of photoreceptors, circuitry taking input from the single luminance-sensitive neuron type L3 implements gain control at fast and slow timescales. This computation is bidirectional in that it prevents underestimation of contrasts in low luminance and overestimation in high luminance. An algorithmic model disentangles these multifaceted contributions and shows that the bidirectional gain control occurs at both timescales. The model implements a nonlinear interaction of luminance and contrast to achieve gain correction at fast timescales and a dark-sensitive channel to improve the detection of dim stimuli at slow timescales. Together, our work demonstrates how a single neuronal channel performs diverse computations to implement gain control at multiple timescales that are together important for navigation in natural environments.

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Section: Discussionmentioning

confidence: 99%

Multifaceted luminance gain control beyond photoreceptors inDrosophila

Ketkar

Shao

Gjorgjieva

et al. 2023

Preprint

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“…cGMP-mediated opening of CNG channels results in calcium influx; intracellular calcium feeds back via calmodulin to modulate CNG channel properties (53)(54)(55)(56)(57). This modulation plays a critical role in regulating adaptation in sensory neurons (12,58). The TAX-2 and TAX-4 CNG thermotransduction channel subunits have been reported to not contain calcium-calmodulin binding sites (59).…”

Section: Phosphorylation Of the Cng-3 But Not Tax-2 Channel Subunit C...mentioning

confidence: 99%

Feedforward and feedback mechanisms cooperatively regulate rapid experience-dependent response adaptation in a single thermosensory neuron type

Hill,

Sengupta

2023

Preprint

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Sensory adaptation allows neurons to adjust their sensitivity and responses based on recent experience. The mechanisms that mediate continuous adaptation to stimulus history over seconds to hours long timescales, and whether these mechanisms can operate within a single sensory neuron type, are unclear. The single pair of AFD thermosensory neurons inC. elegansexhibits experience-dependent plasticity in their temperature response thresholds on both minutes- and hours-long timescales upon a temperature upshift. While long-term response adaptation requires changes in gene expression in AFD, the mechanisms driving rapid response plasticity are unknown. Here, we show that rapid thermosensory response adaptation in AFD is mediated via cGMP and calcium-dependent feedforward and feedback mechanisms operating at the level of primary thermotransduction. We find that either of two thermosensor receptor guanylyl cyclases (rGCs) alone is sufficient to drive rapid adaptation, but that each rGC drives adaptation at different rates. rGC-driven adaptation is mediated in part via phosphorylation of their intracellular domains, and calcium-dependent feedback regulation of basal cGMP levels via a neuronal calcium sensor protein. In turn, cGMP levels feedforward via cGMP-dependent protein kinases to phosphorylate a specific subunit of the cGMP-gated thermotransduction channel to further regulate rapid adaptation. Our results identify multiple molecular pathways that act in AFD to ensure rapid adaptation to a temperature change, and indicate that the deployment of both transcriptional and non-transcriptional mechanisms within a single sensory neuron type can contribute to continuous sensory adaptation.Significance statementThe nervous system must continuously adapt to the sensory environment in order to adjust response sensitivity. Although both short- and long-term response adaptation has been reported to occur within sensory neurons themselves, how temporally distinct plasticity mechanisms are coordinated within single sensory neurons is unclear. We previously showed that long-term adaptation of temperature responses in the single AFD thermosensory neuron pair inC. elegansis mediated via gene expression changes in this neuron type. Here we show that multiple second messenger-driven feedforward and feedback mechanisms act to drive rapid thermosensory adaptation in AFD. Our results indicate that modulation of thermotransduction molecules via both transcriptional and non-transcriptional mechanisms contribute to distinct temporal phases of adaptation in a single sensory neuron type.

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“…Though the astounding variety of smelling organs may seem diverse, the general features of olfactory systems are conserved and share several invariable features which allow for specific and sensitive sampling of broad ranges of odors (Eisthen, 1997;Krieger and Breer, 1999;Ache and Young, 2005;Eisthen and Polese, 2007;Ng et al, 2020). It has long been noted that even disparate olfactory tissues such as mammalian olfactory mucosa and arthropod sensilla display striking similarities in olfactory transduction and structural constraint (Shirsat and Siddiqi, 1993;Abbas and Vinberg, 2021). With respect to the cellular repertoire, olfactory organs are always composed of odorant receptor-equipped sensory neurons innervating an epithelium, and a lesser-explored set of auxiliary cells that co-arise in development, which remain closely apposed to their corresponding neurons, and are thought to play roles in maintaining and potentiating the ability of neurons to perform their sensory function (Schmidt and Benton, 2020).…”

Section: Introductionmentioning

confidence: 99%

Functional Interaction Between Drosophila Olfactory Sensory Neurons and Their Support Cells

Prelic

Mahadevan

Venkateswaran

et al. 2022

Front. Cell. Neurosci.

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Insects detect volatile chemicals using antennae, which house a vast variety of olfactory sensory neurons (OSNs) that innervate hair-like structures called sensilla where odor detection takes place. In addition to OSNs, the antenna also hosts various support cell types. These include the triad of trichogen, tormogen, and thecogen support cells that lie adjacent to their respective OSNs. The arrangement of OSN supporting cells occurs stereotypically for all sensilla and is widely conserved in evolution. While insect chemosensory neurons have received considerable attention, little is known about the functional significance of the cells that support them. For instance, it remains unknown whether support cells play an active role in odor detection, or only passively contribute to homeostasis, e.g., by maintaining sensillum lymph composition. To investigate the functional interaction between OSNs and support cells, we used optical and electrophysiological approaches in Drosophila. First, we characterized the distribution of various supporting cells using genetic markers. By means of an ex vivo antennal preparation and genetically-encoded Ca2+ and K+ indicators, we then studied the activation of these auxiliary cells during odor presentation in adult flies. We observed acute responses and distinct differences in Ca2+ and K+ fluxes between support cell types. Finally, we observed alterations in OSN responses upon thecogen cell ablation in mature adults. Upon inducible ablation of thecogen cells, we notice a gain in mechanical responsiveness to mechanical stimulations during single-sensillum recording, but a lack of change to the neuronal resting activity. Taken together, these results demonstrate that support cells play a more active and responsive role during odor processing than previously thought. Our observations thus reveal that support cells functionally interact with OSNs and may be important for the extraordinary ability of insect olfactory systems to dynamically and sensitively discriminate between odors in the turbulent sensory landscape of insect flight.

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Transduction and Adaptation Mechanisms in the Cilium or Microvilli of Photoreceptors and Olfactory Receptors From Insects to Humans

Cited by 25 publications

References 235 publications

Multifaceted luminance gain control beyond photoreceptors inDrosophila

Multifaceted luminance gain control beyond photoreceptors inDrosophila

Feedforward and feedback mechanisms cooperatively regulate rapid experience-dependent response adaptation in a single thermosensory neuron type

Functional Interaction Between Drosophila Olfactory Sensory Neurons and Their Support Cells

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