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 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 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.

Primary Afferent Neurons Innervating Guinea Pig Dura

1997 ◽  
Vol 77 (1) ◽  
pp. 299-308 ◽  
Author(s):  
Geoffrey M. Bove ◽  
Michael A. Moskowitz
Keyword(s):  
Guinea Pig ◽  
Superior Sagittal Sinus ◽  
Receptive Fields ◽  
Mechanical Stimuli ◽  
Afferent Neurons ◽  
Primary Afferent Neurons ◽  
Primary Afferent ◽  
Response Properties ◽  
Thermal Thresholds ◽  
Sagittal Sinus

Bove, Geoffrey M. and Michael A. Moskowitz. Primary Afferent Neurons Innervating Guinea Pig Dura. J. Neurophysiol. 77: 299–308, 1997. We made recordings from filaments of guinea pig nasociliary nerve to study response properties of afferent axons innervating the anterior superior sagittal sinus and surrounding dura mater. We analyzed 38 units in 14 experiments. Units were initially located with the use of mechanical stimuli, and were then characterized by their conduction velocity and sensitivities to mechanical, thermal, and chemical stimuli. Single-unit recordings revealed innervation of dura and superior sagittal sinus by slowly conducting axons, mostly in the unmyelinated range. The receptive fields were 1–30 mm2, and typically had one to three punctate spots of highest sensitivity. All units tested responded to topical application of chemical agents. Ninety-seven percent of units responded to 10−5 M capsaicin, 79% responded to a mixture of inflammatory mediators, and 37% responded to an acidic buffer (pH 5). These data underline the importance of chemical sensitivity in intracranial sensation. Heat and cold stimuli evoked responses in 56 and 41% of units tested, respectively. Although the response patterns during heating were typical of polymodal nociceptors innervating other tissues, the thresholds were lower than for other tissues (32.3–42°C). Cooling led to a phasic discharge, with thresholds between 25 and 32°C. Although units had different combinations of responses to mechanical, chemical, and thermal stimuli, when grouped by their sensitivities the groups did not differ regarding mechanical thresholds or presence of ongoing activity. This suggests that meningeal primary afferents are relatively homogeneous. Sensitivities of these units are in general consistent with nociceptors, although the thermal thresholds differ. These data provide the first detailed report of response properties of intracranial primary afferent units, likely to be involved in transmission of nociception and possibly mediation of intracranial pain.

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.

Frequency Response Properties of Lateral Line Superficial Neuromasts in a Vocal Fish, With Evidence for Acoustic Sensitivity

2002 ◽  
Vol 88 (3) ◽  
pp. 1252-1262 ◽  
Author(s):  
Matthew S. Weeg ◽  
Andrew H. Bass
Keyword(s):  
Frequency Response ◽  
Lateral Line ◽  
Sensory System ◽  
Spike Rate ◽  
Pass Band ◽  
Lateral Line System ◽  
Line System ◽  
Response Properties ◽  
Lateral Line Nerve ◽  
Direct Demonstration

The mechanosensory lateral line of fish is a hair cell based sensory system that detects water motion using canal and superficial neuromasts. The trunk lateral line of the plainfin midshipman fish, Porichthys notatus, only has superficial neuromasts. The posterior lateral line nerve (PLLn) therefore innervates trunk superficial neuromasts exclusively and provides the opportunity to investigate the physiological responses of these receptors without the confounding influence of canal organs. We recorded single-unit activity from PLLn primary afferents in response to a vibrating sphere stimulus calibrated to produce an equal velocity across frequencies. Threshold tuning, isovelocity, and input/output curves were constructed using spike rate and vector strength, a measure of phase locking of spike times to the stimulus waveform. All units responded maximally to frequencies of 20–50 Hz. Units were classified as low-pass, band-pass, broadly tuned, or complex based on the shapes of tuning and isovelocity curves between 20 and 100 Hz. A 100 Hz stimulus caused an increase in spike rate in almost 50%, and significant synchronization in >80%, of all units. Midshipman vocalizations contain significant energy at and below 100 Hz, so these results demonstrate that the midshipman peripheral lateral line system can encode these acoustic signals. These results provide the first direct demonstration that units innervating superficial neuromasts in a teleost fish have heterogeneous frequency response properties, including an upper range of sensitivity that overlaps spectral peaks of behaviorally relevant acoustic stimuli.

Hindbrain signal processing in the lateral line system of the dwarf scorpionfish Scopeana papillosus

1996 ◽  
Vol 199 (4) ◽  
pp. 893-899 ◽  
Author(s):  
J Montgomery ◽  
D Bodznick ◽  
M Halstead
Keyword(s):  
Signal Processing ◽  
Spontaneous Activity ◽  
Lateral Line ◽  
Primary Afferents ◽  
Lateral Line System ◽  
Strong Suppression ◽  
Primary Afferent ◽  
Line System ◽  
Response Characteristics ◽  
Tonic Response

Recordings were made from primary afferent fibres and secondary projection neurones (crest cells) in the mechanosensory lateral line system of the dwarf scorpionfish. Crest cells were identified by antidromic stimulation from the contralateral midbrain. Differences between primary afferent fibre and crest cell response characteristics are indicative of signal processing by the neuronal circuitry of the medial octavolateralis nucleus. There are a number of differences between primary afferent fibres and crest cells. Primary afferents have relatively high levels of spontaneous activity (mean close to 40 impulses s-1) and many of them are strongly modulated by ventilation. By contrast, crest cells have a much lower rate of spontaneous activity that is not obviously modulated by ventilation. Primary afferents show a simple tonic response to a maintained stimulus, whereas crest cells show a variety of temporal response properties, but in general show a phasic/tonic response to the same prolonged stimulus. Afferents are most sensitive to frequencies of stimulation around 100 Hz; in contrast, crest cells show a strong suppression of activity at this frequency. Crest cells are most responsive around 50 Hz. These afferent/secondary comparisons show similarities with those reported for allied electrosensory and auditory pathways.

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