Motor Behavior Selectively Inhibits Hair Cells Activated by Forward Motion in the Lateral Line of Zebrafish

Pichler, Paul; Lagnado, Leon

doi:10.1016/j.cub.2019.11.020

Cited by 46 publications

(82 citation statements)

References 52 publications

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“…Viewed this way, the emphasis on h-t flow processing that we observe is unsurprising, since this type of flow would be more common, and likely more ethologically relevant, to larval zebrafish. Recent observations of specific silencing of the h-t flow response at the neuromast level by efferent copies during self-motion also support an ethological relevance to the h-t flow (Pichler and Lagnado, 2020). However, the paralyzing agent we used blocks the cholinergic receptors that mediate this silencing by the motor neurons, and we did not observe swim bouts as a result of our stimuli.…”

Section: Coding Of Detailed Information About H-t Water Flowsupporting

confidence: 74%

Brain-Wide Mapping of Water Flow Perception in Zebrafish

et al. 2020

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Information about water flow, detected by lateral line organs, is critical to the behavior and survival of fish and amphibians. While certain aspects of water flow processing have been revealed through electrophysiology, we lack a comprehensive description of the neurons that respond to water flow and the network that they form. Here, we use brain-wide calcium imaging in combination with microfluidic stimulation to map out, at cellular resolution, neuronal responses involved in perceiving and processing water flow information in larval zebrafish. We find a diverse array of neurons responding to head-totail (h-t) flow, tail-to-head (t-h) flow, or both. Early in this pathway, in the lateral line ganglia, neurons respond almost exclusively to the simple presence of h-t or t-h flow, but later processing includes neurons responding specifically to flow onset, representing the accumulated displacement of flow during a stimulus, or encoding the speed of the flow. The neurons reporting on these more nuanced details are located across numerous brain regions, including some not previously implicated in water flow processing. A graph theory-based analysis of the brain-wide water flow network shows that a majority of this processing is dedicated to h-t flow detection, and this is reinforced by our finding that details like flow velocity and the total accumulated flow are only encoded for the h-t direction. The results represent the first brain-wide description of processing for this important modality, and provide a departure point for more detailed studies of the flow of information through this network.

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Section: Coding Of Detailed Information About H-t Water Flowsupporting

confidence: 74%

Brain-Wide Mapping of Water Flow Perception in Zebrafish

et al. 2020

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“…However, only one efferent fiber contacts all HC of a single neuromast (Faucherre et al, 2009;Dow et al, 2018). Moreover, during fictive locomotion presynaptic activity across all efferent synapses within a neuromast are synchronously activated (Pichler and Lagnado, 2020). Similarly, in our experiments ACh-mediated effects were observed in HC irrespective of their polarity and the median magnitude of inhibition in both cases showed no significant difference.…”

Section: Discussionsupporting

confidence: 60%

“…Scyliorhynus, inhibits spontaneous and evoked activity of afferents by generating inhibitory postsynaptic potentials in HC Roberts and Russell, 1972;Flock and Russell, 1976). In zebrafish, activation of cholinergic efferents suppresses glutamate release from HC (Pichler and Lagnado, 2020) and inhibits afferent activity (Lunsford et al, 2019). This most likely results from ACh-evoked hyperpolarization of HC and reduced Ca 2+ influx through voltageactivated Ca 2+ channels.…”

Section: Stimulation Of Cholinergic Efferents In the Ll Of Xenopus Bmentioning

confidence: 99%

“…In particular, efferent stimulation to the LL and the inner ear leads to inhibition of afferent transmission Roberts and Russell, 1972;Flock and Russell, 1976;Lunsford et al, 2019;Pichler and Lagnado, 2020), thus suggesting similar synaptic mechanisms. This is most likely brought about by cholinergic efferent fibers (Dawkins et al, 2005;Zhang et al, 2018) directly contacting the base of LL HC (Dow et al, 2018), similar to what has been described for MOC efferents.…”

Section: Introductionmentioning

confidence: 99%

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Unravelling the molecular players at the cholinergic efferent synapse of the zebrafish lateral line

Freixas

Moglie

Castagnola

et al. 2020

Preprint

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AbstractThe lateral line (LL) is a sensory system that allows fish and amphibians to detect water currents. LL responsiveness to external stimuli is modulated by descending efferent neurons. LL efferent modulation aids the animal to distinguish between external and self-generated stimuli, maintaining sensitivity to relevant cues. One of the main components of the efferent system is cholinergic, the activation of which inhibits afferent activity. Since LL hair cells (HC) share structural, functional and molecular similarities with those of the cochlea, one could propose that the receptor at the LL efferent synapse is a α9α10 nicotinic cholinergic one (nAChR). However, the identity of the molecular players underlying acetylcholine (ACh)-mediated inhibition in the LL remain unknown. Surprisingly, through the analysis of single-cell expression data and in situ hybridization, we describe that α9, but not α10 subunits, are enriched in zebrafish HC. Moreover, the heterologous expression of zebrafish α9 subunits indicates that α9 homomeric receptors are functional and exhibit robust ACh-gated currents which are blocked by α-Bungarotoxin (α-Btx). In addition, in vivo Ca2+ imaging on mechanically-stimulated zebrafish LL HC showed that ACh elicits a decrease in evoked Ca2+ signals, irrespective of HC polarity. This effect was blocked by both α-Btx and apamin, indicating coupling of ACh mediated effects to SK potassium channels. Collectively, our results indicate that an α9-containing (α9*) nAChR operates at the zebrafish LL efferent synapse. Moreover, the activation of α9* nAChRs most likely leads to LL HC hyperpolarization served by the ACh-dependent activation of Ca2+-dependent SK potassium channels.Significance StatementFishes and amphibians have a mechanosensory system, the lateral line (LL), which serves to detect hydromechanical variations around the animal’s body. The LL receives descending efferent innervation from the brain that modulates its responsiveness to external stimuli. LL efferent inhibition is mediated by ACh, however the identity of the molecular players at the LL efferent synapse is unknown. Here we demonstrate that a nicotinic cholinergic receptor (nAChR) composed of α9 subunits operates at the LL efferent synapse. Activation of α9-containing (α9*) nAChRs leads to LL hair cell hyperpolarization. The inhibitory signature of this process is brought about by the subsequent activation of Ca2+-dependent potassium SK channels, functionally coupled to α9* nAChRs.

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“…Although it has been shown that the connections between afferent neurons and hair-cell bundles of the LL neuromast develop independently of experience in larval zebrafish [Nagiel et al, 2009], this sensory organ shows several filtering properties whose development might depend on experience. For instance, efferent copies of forward motion suppress synaptic transmission in lateral line hair cells [Pichler and Lagnado, 2020], and canal neuromasts are capable of sensing water vibrations even against a background of unidirectional water flow [Engelmann et al, 2002]. Such fine-tuning of LL sensing under specialized conditions could be shaped through the sensory experiences of the presence of conspecifics.…”

Section: Discussionmentioning

confidence: 99%

Early-life social experience shapes social avoidance reactions in larval zebrafish

Groneberg

Marques

Martins

et al. 2020

Preprint

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Highlights:• Larval zebrafish raised in isolation show enhanced social avoidance reactions • Enhanced avoidance is composed of increased avoidance distances and usage of high acceleration escape swims• The lateral line sensory organ is necessary and sufficient for the increased usage of high acceleration escape swims Summary Social experiences greatly define successive social behavior. Lack of such experiences, especially during critical phases of development, can severely impede the ability to behave adequately in social contexts. To date it is not well characterized how early-life social isolation leads to social deficits and impacts development. In many model species, it is challenging to fully control social experiences, because they depend on parental care. Moreover, complex social behaviors involve multiple sensory modalities, contexts, and actions. Hence, when studying social isolation effects, it is particularly important to parse apart social deficits from general developmental effects, such as abnormal motor learning. Here, we characterized how social experiences during early development of zebrafish larvae modulate their social behavior, at one week of age, when social avoidance reactions can be measured as discrete swim events. We show that raising larvae in social isolation leads to enhanced social avoidance, in terms of reaction distance and reaction strength. Specifically, larvae raised in isolation use a high-acceleration escape swim bout, the short latency C-start, more frequently during social interactions. These behavioral differences are absent in non-social contexts. By ablating the lateral line and presenting the fish with local water vibrations, we show that lateral line inputs are both necessary and sufficient to drive enhanced social avoidance reactions. Taken together, our results show that social experience during development is a critical factor in shaping mechanosensory avoidance reactions in larval zebrafish.An important aspect of behavior is that it is adaptive and can change according to previous 2 outcomes of the actions of the self or others. During early development, as the nervous sys-3 tem builds and refines its connections, an animal is particularly sensitive to external sensory 4 input, or lack thereof (e.g. reviewed by Andersen [2003]). Social experiences during early 5 development can have long lasting effects on social and other behaviors, as shown by the dev-6

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Motor Behavior Selectively Inhibits Hair Cells Activated by Forward Motion in the Lateral Line of Zebrafish

Cited by 46 publications

References 52 publications

Brain-Wide Mapping of Water Flow Perception in Zebrafish

Brain-Wide Mapping of Water Flow Perception in Zebrafish

Unravelling the molecular players at the cholinergic efferent synapse of the zebrafish lateral line

Early-life social experience shapes social avoidance reactions in larval zebrafish

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