scholarly journals Efferent Modulation of Spontaneous Lateral Line Activity During and after Zebrafish Motor Commands

2019 ◽  
Author(s):  
Elias T. Lunsford ◽  
Dimitri A. Skandalis ◽  
James C. Liao
Keyword(s):  
Motor Activity ◽  
Lateral Line ◽  
Spike Frequency ◽  
The Body ◽  
Corollary Discharge ◽  
Lateral Line System ◽  
Afferent Neurons ◽  
Line System ◽  
Larval Zebrafish ◽  
Efferent Neurons

AbstractAccurate sensory processing during movement requires the animal to distinguish between external (exafferent) and self-generated (reafferent) stimuli to maintain sensitivity to biologically relevant cues. The lateral line system in fishes is a mechanosensory organ that experiences reafferent sensory feedback via detection of fluid motion relative to the body generated during behaviors such as swimming. For the first time in larval zebrafish (Danio rerio), we employed simultaneous recordings of lateral line and motor activity to reveal the activity of afferent neurons arising from endogenous feedback from hindbrain efferent neurons during locomotion. Frequency of spontaneous spiking in posterior lateral line afferent neurons decreased during motor activity and was absent for more than half of swimming trials. Targeted photoablation of efferent neurons abolished the afferent inhibition that was correlated to swimming, indicating that inhibitory efferent neurons are necessary for modulating lateral line sensitivity during locomotion. We monitored calcium activity with Tg(elav13:GCaMP6s) fish and found synchronous activity between putative cholinergic efferent neurons and motor neurons. We examined correlates of motor activity to determine which may best predict the attenuation of afferent activity and therefore what components of the motor signal are translated through the corollary discharge. Swim duration was most strongly correlated to the change in afferent spike frequency. Attenuated spike frequency persisted past the end of the fictive swim bout, suggesting that corollary discharge also affects the glide phase of burst and glide locomotion. The duration of the glide in which spike frequency was attenuated increased with swim duration but decreased with motor frequency. Our results detail a neuromodulatory mechanism in larval zebrafish that adaptively filters self-generated flow stimuli during both the active and passive phases of locomotion.

scholarly journals Efferent modulation of spontaneous lateral line activity during and after zebrafish motor commands

2019 ◽  
Vol 122 (6) ◽  
pp. 2438-2448 ◽  
Author(s):  
Elias T. Lunsford ◽  
Dimitri A. Skandalis ◽  
James C. Liao
Keyword(s):  
Motor Activity ◽  
Lateral Line ◽  
Spike Frequency ◽  
Corollary Discharge ◽  
Lateral Line System ◽  
Afferent Neurons ◽  
Afferent Activity ◽  
Larval Zebrafish ◽  
Efferent Neurons ◽  
First Time

Accurate sensory processing during movement requires the animal to distinguish between external (exafferent) and self-generated (reafferent) stimuli to maintain sensitivity to biologically relevant cues. The lateral line system in fishes is a mechanosensory organ that experiences reafferent sensory feedback, via detection of fluid motion relative to the body generated during behaviors such as swimming. For the first time in larval zebrafish ( Danio rerio), we employed simultaneous recordings of lateral line and motor activity to reveal the activity of afferent neurons arising from endogenous feedback from hindbrain efferent neurons during locomotion. Frequency of spontaneous spiking in posterior lateral line afferent neurons decreased during motor activity and was absent for more than half of swimming trials. Targeted photoablation of efferent neurons abolished the afferent inhibition that was correlated to swimming, indicating that inhibitory efferent neurons are necessary for modulating lateral line sensitivity during locomotion. We monitored calcium activity with Tg(elav13:GCaMP6s) fish and found synchronous activity between putative cholinergic efferent neurons and motor neurons. We examined correlates of motor activity to determine which may best predict the attenuation of afferent activity and therefore what components of the motor signal are translated through the corollary discharge. Swim duration was most strongly correlated to the change in afferent spike frequency. Attenuated spike frequency persisted past the end of the fictive swim bout, suggesting that corollary discharge also affects the glide phase of burst and glide locomotion. The duration of the glide in which spike frequency was attenuated increased with swim duration but decreased with motor frequency. Our results detail a neuromodulatory mechanism in larval zebrafish that adaptively filters self-generated flow stimuli during both the active and passive phases of locomotion. NEW & NOTEWORTHY For the first time in vivo, we quantify the endogenous effect of efferent activity on afferent gain control in a vertebrate hair cell system during and after locomotion. We believe that this pervasive effect has been underestimated when afferent activity of octavolateralis systems is characterized in the current literature. We further identify a refractory period out of phase with efferent control and place this gain mechanism in the context of gliding behavior of freely moving animals.

scholarly journals Organization and physiology of posterior lateral line afferent neurons in larval zebrafish

2010 ◽  
Vol 6 (3) ◽  
pp. 402-405 ◽  
Author(s):  
James C. Liao
Keyword(s):  
Lateral Line ◽  
Spatial Relationship ◽  
Genetic System ◽  
The Body ◽  
Lateral Line System ◽  
Afferent Neurons ◽  
Patch Clamp Recording ◽  
Line System ◽  
Larval Zebrafish ◽  
Posterior Lateral Line

The lateral line system of larval zebrafish can translate hydrodynamic signals from the environment to guide body movements. Here, I demonstrate a spatial relationship between the organization of afferent neurons in the lateral line ganglion and the innervation of neuromasts along the body. I developed a whole cell patch clamp recording technique to show that afferents innervate multiple direction-sensitive neuromasts, which are sensitive to low fluid velocities. This work lays the foundation to integrate sensory neuroscience and the hydrodynamics of locomotion in a model genetic system.

scholarly journals Frequency response properties of primary afferent neurons in the posterior lateral line system of larval zebrafish

2015 ◽  
Vol 113 (2) ◽  
pp. 657-668 ◽  
Author(s):  
Rafael Levi ◽  
Otar Akanyeti ◽  
Aleksander Ballo ◽  
James C. Liao
Keyword(s):  
Lateral Line ◽  
Sine Wave ◽  
Afferent Neuron ◽  
Lateral Line System ◽  
Afferent Neurons ◽  
Primary Afferent Neurons ◽  
Primary Afferent ◽  
Line System ◽  
Response Properties ◽  
Larval Zebrafish

The ability of fishes to detect water flow with the neuromasts of their lateral line system depends on the physiology of afferent neurons as well as the hydrodynamic environment. Using larval zebrafish ( Danio rerio), we measured the basic response properties of primary afferent neurons to mechanical deflections of individual superficial neuromasts. We used two types of stimulation protocols. First, we used sine wave stimulation to characterize the response properties of the afferent neurons. The average frequency-response curve was flat across stimulation frequencies between 0 and 100 Hz, matching the filtering properties of a displacement detector. Spike rate increased asymptotically with frequency, and phase locking was maximal between 10 and 60 Hz. Second, we used pulse train stimulation to analyze the maximum spike rate capabilities. We found that afferent neurons could generate up to 80 spikes/s and could follow a pulse train stimulation rate of up to 40 pulses/s in a reliable and precise manner. Both sine wave and pulse stimulation protocols indicate that an afferent neuron can maintain their evoked activity for longer durations at low stimulation frequencies than at high frequencies. We found one type of afferent neuron based on spontaneous activity patterns and discovered a correlation between the level of spontaneous and evoked activity. Overall, our results establish the baseline response properties of lateral line primary afferent neurons in larval zebrafish, which is a crucial step in understanding how vertebrate mechanoreceptive systems sense and subsequently process information from the environment.

scholarly journals Afferent and motoneuron activity in response to single neuromast stimulation in the posterior lateral line of larval zebrafish

2014 ◽  
Vol 112 (6) ◽  
pp. 1329-1339 ◽  
Author(s):  
Melanie Haehnel-Taguchi ◽  
Otar Akanyeti ◽  
James C. Liao
Keyword(s):  
Lateral Line ◽  
Transfer Functions ◽  
Spike Rate ◽  
The Body ◽  
Neuron Activity ◽  
Afferent Neuron ◽  
Lateral Line System ◽  
Line System ◽  
Larval Zebrafish ◽  
Motoneuron Activity

The lateral line system of fishes contains mechanosensory receptors along the body surface called neuromasts, which can detect water motion relative to the body. The ability to sense flow informs many behaviors, such as schooling, predator avoidance, and rheotaxis. Here, we developed a new approach to stimulate individual neuromasts while either recording primary sensory afferent neuron activity or swimming motoneuron activity in larval zebrafish ( Danio rerio). Our results allowed us to characterize the transfer functions between a controlled lateral line stimulus, its representation by primary sensory neurons, and its subsequent behavioral output. When we deflected the cupula of a neuromast with a ramp command, we found that the connected afferent neuron exhibited an adapting response which was proportional in strength to deflection velocity. The maximum spike rate of afferent neurons increased sigmoidally with deflection velocity, with a linear range between 0.1 and 1.0 μm/ms. However, spike rate did not change when the cupula was deflected below 8 μm, regardless of deflection velocity. Our findings also reveal an unexpected sensitivity in the larval lateral line system: stimulation of a single neuromast could elicit a swimming response which increased in reliability with increasing deflection velocities. At high deflection velocities, we observed that lateral line evoked swimming has intermediate values of burst frequency and duty cycle that fall between electrically evoked and spontaneous swimming. An understanding of the sensory capabilities of a single neuromast will help to build a better picture of how stimuli are encoded at the systems level and ultimately translated into behavior.

scholarly journals Physiology of afferent neurons in larval zebrafish provides a functional framework for lateral line somatotopy

2012 ◽  
Vol 107 (10) ◽  
pp. 2615-2623 ◽  
Author(s):  
James C. Liao ◽  
Melanie Haehnel
Keyword(s):  
Firing Rate ◽  
Lateral Line ◽  
Input Resistance ◽  
Lateral Line System ◽  
Spontaneous Firing ◽  
Afferent Neurons ◽  
Line System ◽  
Larval Zebrafish ◽  
Posterior Lateral Line ◽  
Spontaneous Firing Rate

Fishes rely on the neuromasts of their lateral line system to detect water flow during behaviors such as predator avoidance and prey localization. Although the pattern of neuromast development has been a topic of detailed research, we still do not understand the functional consequences of its organization. Previous work has demonstrated somatotopy in the posterior lateral line, whereby afferent neurons that contact more caudal neuromasts project more dorsally in the hindbrain than those that contact more rostral neuromasts (Gompel N, Dambly-Chaudiere C, Ghysen A. Development 128: 387–393, 2001). We performed patch-clamp recordings of afferent neurons that contact neuromasts in the posterior lateral line of anesthetized, transgenic larval zebrafish ( Danio rerio) to show that larger cells are born earlier, have a lower input resistance, a lower spontaneous firing rate, and tend to contact multiple neuromasts located closer to the tail than smaller neurons, which are born later, have a higher input resistance, a higher spontaneous firing rate, and tend to contact single neuromasts. We suggest that early-born neurons are poised to detect large stimuli during the initial stages of development. Later-born neurons are more easily driven to fire and thus likely to be more sensitive to local, weaker flows. Afferent projections onto identified glutamatergic regions in the hindbrain lead us to hypothesize a novel mechanism for lateral line somatotopy. We show that afferent fibers associated with tail neuromasts respond to stronger stimuli and are wired to dorsal hindbrain regions associated with Mauthner-mediated escape responses and fast, avoidance swimming. The ability to process flow stimuli by circumventing higher-order brain centers would ease the task of processing where speed is of critical importance. Our work lays the groundwork to understand how the lateral line translates flow stimuli into appropriate behaviors at the single cell level.

scholarly journals Initiation of locomotion by lateral line photoreceptors in lamprey: behavioural and neurophysiological studies

1995 ◽  
Vol 198 (12) ◽  
pp. 2581-2591 ◽  
Author(s):  
T G Deliagina ◽  
F Ullén ◽  
M-J. Gonzalez ◽  
H Ehrsson ◽  
G N Orlovsky ◽  
...  
Keyword(s):  
Lateral Line ◽  
The Body ◽  
Lateral Line System ◽  
Tail Region ◽  
Directional Bias ◽  
Line System ◽  
Lateral Line Nerve ◽  
Neurophysiological Studies ◽  
Behavioural Experiments ◽  
The Right

The lateral line system of lampreys includes photoreceptors distributed in the skin of the tail region. These are innervated by the trunk lateral line nerves, and the afferents terminate bilaterally in the medial octavolateral nucleus, crossing the midline through the cerebellar commissure. Stimulation of the dermal photoreceptors by tail illumination initiates locomotion. The present study was performed to characterize the response to illumination in larval and adult lampreys in detail and to elucidate the neuronal pathways responsible for the activation of locomotion. In both larval and adult quiescent lampreys, the response to unilateral illumination of the tail was found to consist of an initial turn followed by rectilinear swimming. The sign and magnitude of the turning angle were not correlated with the laterality of the optic stimulus. In mechanically restrained lampreys, spinalized at the level of segments 15­20, tail illumination evoked a complex motor response in the rostral part of the body, with switches between different patterns of coordination (turns in different directions, locomotion, and turns combined with locomotion). Thus, the response to tail illumination is not a simple reflex, but includes a behavioural choice. Reticulospinal neurones play a crucial role in the initiation of locomotion in lampreys. The response to unilateral tail illumination in rhombencephalic reticular cells was studied with extracellular single-unit recordings. It was found that neurones in the middle and posterior rhombencephalic reticular nuclei were activated bilaterally. Tonic activity or slow bursts (<0.5 Hz) were evoked, in some cases lasting up to 60 s after the stimulation. The response remained bilateral after transection of one lateral line nerve and the cerebellar commissure. Afferents from one side can thus activate reticulospinal cells on both sides through a pathway outside the cerebellar commissure. This bilateral activation of reticulospinal neurones is presumably responsible for the activation of spinal locomotor networks, without any directional bias to the left or the right side, and for the rectilinear swimming observed in behavioural experiments. In the caudal part of the termination area of the lateral line nerve afferents, neurones with contralateral projections were retrogradely stained with horseradish peroxidase. These neurones appear to be likely candidates for mediating the contralateral effects of the lateral line fibres.

The Ionic Composition of the Lateral-Line Canal Fluid of Dogfish

1972 ◽  
Vol 52 (3) ◽  
pp. 653-659 ◽  
Author(s):  
Jennifer D. Liddicoat ◽  
B. L. Roberts
Keyword(s):  
Lateral Line ◽  
Body Surface ◽  
Ionic Composition ◽  
The Body ◽  
Lateral Line System ◽  
Sense Organs ◽  
Canal System ◽  
Line System ◽  
Aquatic Vertebrates ◽  
Definite Pattern

The sense organs of the lateral-line system of lower aquatic vertebrates are mechanoreceptors which respond to water movements. They are distributed over the body, usually in lines which form a definite pattern on the head and along each side of the trunk. In the Cyclostomes the sense organs project from the body surface ('free neuromasts'); in other aquatic vertebrates they are usually housed in canals which are sunk into the dermis and which open at regular intervals to the exterior, although in some teleosts and in all modern amphibia the canal system has been secondarily lost and the neuromasts are once again situated externally.

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