Lateral line sensitivity in free swimming toadfish,<i>Opsanus tau</i>

Mensinger, Allen F.; Wert, Jacey C. Van; Rogers, Loranzie S.

doi:10.1242/jeb.190587

Cited by 19 publications

(17 citation statements)

References 31 publications

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“…We still know relatively little about efferent modulation in freely-swimming fishes, where hydrodynamic stimuli from swimming can further impact afferent activity, but we now have a greater appreciation for the complex relationship between sensory and motor systems. In freely moving fish, afferent spike frequencies increase both during swimming and during feeding strikes (Palmer et al 2005; Palmer et al 2003; Ayali et al 2009; Mensinger et al 2019). This is consistent with our observation that efferent activity only partially suppresses spontaneous spike rates.…”

Section: Discussionmentioning

confidence: 99%

“…Fishes sense perturbations in the fluid environment through the lateral line, a sensory organ on the body surface that translates fluid motion relative to the body into neural signals essential for navigation (Olszewski, et al 2012, Suli et al 2012, Oteiza et al 2017), predator avoidance, prey capture (McHenry et al 2009; Stewart et al 2013), and schooling (Mekdara et al 2018). However, since water motions are also self-generated by behaviors such as swimming (Palmer et al 2003; Ayali et al 2009; Mensinger et al 2019), respiration (Montgomery et al 1996; Montgomery and Bodznick 1994; Palmer et al 2003), and feeding (Palmer et al 2005), fishes should possess a mechanism to discriminate such self-generated signals from environmental signals.…”

Section: Introductionmentioning

confidence: 99%

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

Lunsford

Skandalis

Liao

2019

Preprint

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1Accurate sensory processing during movement requires the animal to distinguish between 2 2 3 1 that inhibitory efferent neurons are necessary for modulating lateral line sensitivity during 3 2 locomotion. We monitored calcium activity with Tg(elav13:GCaMP6s) fish and found 3 3 synchronous activity between putative cholinergic efferent neurons and motor neurons. We 3 4 examined correlates of motor activity to determine which may best predict the attenuation of 3 5 afferent activity and therefore what components of the motor signal are translated through the 3 6 corollary discharge. Swim duration was most strongly correlated to the change in afferent spike 3 7 frequency. Attenuated spike frequency persisted past the end of the fictive swim bout, suggesting 3 8 that corollary discharge also affects the glide phase of burst and glide locomotion. The duration 3 9of the glide in which spike frequency was attenuated increased with swim duration but decreased 4 0 with motor frequency. Our results detail a neuromodulatory mechanism in larval zebrafish that 4 1 adaptively filters self-generated flow stimuli during both the active and passive phases of 4 2 locomotion. 4 3 4 4

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Lunsford

Skandalis

Liao

2019

Preprint

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“…Fishes sense perturbations in the fluid environment through the lateral line, a sensory organ on the body surface that translates fluid motion relative to the body into neural signals essential for navigation (Olszewski, et al 2012;Oteiza et al 2017;Suli et al 2012), predator avoidance, prey capture (McHenry et al 2009;Stewart et al 2013), and schooling (Mekdara et al 2018). However, since water motions are also self-generated by behaviors such as swimming (Ayali et al 2009;Mensinger et al 2019;Palmer et al 2003), respiration (Montgomery et al 1996;Montgomery and Bodznick 1994;Palmer et al 2003), and feeding (Palmer et al 2005), fishes should possess a mechanism to discriminate such self-generated signals from environmental signals.…”

Section: Introductionmentioning

confidence: 99%

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

Lunsford

Skandalis

Liao

2019

Journal of Neurophysiology

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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.

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“…Prolonged inhibition during these ongoing behaviors seems unlikely as responses to important external stimuli would be inhibited as well. A recent study in toadfish indeed found that the lateral line system remains sensitive to external stimuli in spite of selfstimulation generated by swimming (Mensinger et al, 2018). It appears that a more dynamic filter would be useful under most circumstances and evidence for predictive cancellation of reafference was briefly reported in the MON of the teleost scorpion fish, but this has not been further studied (Montgomery and Bodznick, 1994).…”

Section: Introductionmentioning

confidence: 99%

“…This could reduce reafference by turning off the receptors during behavior, but the efferents appear only to be activated during very vigorous behaviors that threaten to overdrive receptors (Bodznick, 1989;Roberts and Russell, 1972). The requisite movements of behaviors such as ventilation and swimming cause self-stimulation that drives lateral line primary afferent responses (Montgomery et al, 1996;Russell and Roberts, 1974;Palmer et al, 2005;Ayali et al, 2009;Mensinger et al, 2018). However, second-order cells are not driven by the same self-stimulation, at least in the case of ventilation (Montgomery et al, 1996).…”

Section: Introductionmentioning

confidence: 99%

A cerebellum-like circuit in the lateral line system of fish cancels mechanosensory input associated with its own movements

Perks

Krotinger

Bodznick

2020

Journal of Experimental Biology

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An animal's own movement exerts a profound impact on sensory input to its nervous system. Peripheral sensory receptors do not distinguish externally generated stimuli from stimuli generated by an animal's own behavior (reafference)although the animal often must. One way that nervous systems can solve this problem is to provide movement-related signals (copies of motor commands and sensory feedback) to sensory systems, which can then be used to generate predictions that oppose or cancel out sensory responses to reafference. Here, we studied the use of movement-related signals to generate sensory predictions in the lateral line medial octavolateralis nucleus (MON) of the little skate. In the MON, mechanoreceptive afferents synapse on output neurons that also receive movement-related signals from central sources, via a granule cell parallel fiber system. This parallel fiber system organization is characteristic of a set of so-called cerebellum-like structures. Cerebellum-like structures have been shown to support predictive cancellation of reafference in the electrosensory systems of fish and the auditory system of mice. Here, we provide evidence that the parallel fiber system in the MON can generate predictions that are negative images of (and therefore cancel) sensory input associated with respiratory and fin movements. The MON, found in most aquatic vertebrates, is probably one of the most primitive cerebellum-like structures and a starting point for cerebellar evolution. The results of this study contribute to a growing body of work that uses an evolutionary perspective on the vertebrate cerebellum to understand its functional diversity in animal behavior.

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Lateral line sensitivity in free swimming toadfish,Opsanus tau

Cited by 19 publications

References 31 publications

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

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

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

A cerebellum-like circuit in the lateral line system of fish cancels mechanosensory input associated with its own movements

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