scholarly journals Removing a single neuron in a vertebrate brain forever abolishes an essential behavior

2020 ◽  
Vol 117 (6) ◽  
pp. 3254-3260 ◽  
Author(s):  
Alexander Hecker ◽  
Wolfram Schulze ◽  
Jakob Oster ◽  
David O. Richter ◽  
Stefan Schuster
Keyword(s):  
Single Neuron ◽  
Escape Behavior ◽  
Extended Period ◽  
Escape Performance ◽  
M Cell ◽  
Giant Neuron ◽  
Vertebrate Brain ◽  
Vital Functions ◽  
Natural Predator ◽  
Actual Survival

The giant Mauthner (M) cell is the largest neuron known in the vertebrate brain. It has enabled major breakthroughs in neuroscience but its ultimate function remains surprisingly unclear: An actual survival value of M cell-mediated escapes has never been supported experimentally and ablating the cell repeatedly failed to eliminate all rapid escapes, suggesting that escapes can equally well be driven by smaller neurons. Here we applied techniques to simultaneously measure escape performance and the state of the giant M axon over an extended period following ablation of its soma. We discovered that the axon survives remarkably long and remains still fully capable of driving rapid escape behavior. By unilaterally removing one of the two M axons and comparing escapes in the same individual that could or could not recruit an M axon, we show that the giant M axon is essential for rapid escapes and that its loss means that rapid escapes are also lost forever. This allowed us to directly test the survival value of the M cell-mediated escapes and to show that the absence of this giant neuron directly affects survival in encounters with a natural predator. These findings not only offer a surprising solution to an old puzzle but demonstrate that even complex brains can trust vital functions to individual neurons. Our findings suggest that mechanisms must have evolved in parallel with the unique significance of these neurons to keep their axons alive and connected.

scholarly journals Effects of Temperature Acclimation on a Central Neural Circuit and Its Behavioral Output

2008 ◽  
Vol 100 (6) ◽  
pp. 2997-3008 ◽  
Author(s):  
Theresa M. Szabo ◽  
Ted Brookings ◽  
Thomas Preuss ◽  
Donald S. Faber
Keyword(s):  
Neural Circuit ◽  
Escape Behavior ◽  
Input Resistance ◽  
Temperature Acclimation ◽  
M Cell ◽  
Escape Probability ◽  
Single Action ◽  
Vertebrate Brain ◽  
Behavioral Responsiveness ◽  
The Impact

In this study, we address the impact of temperature acclimation on neuronal properties in the Mauthner (M-) system, a brain stem network that initiates the startle-escape behavior in goldfish. The M-cell can be studied at cellular and behavioral levels, since it is uniquely identifiable physiologically within the intact vertebrate brain, and a single action potential in this neuron determines not only whether a startle response will occur but also the direction of the escape. Using animals acclimated to 15°C as a control, 25°C-acclimated fish showed a significant increase in escape probability and a decrease in the ability to discriminate escape directionality. Intracellular recordings demonstrated that M-cells in this population possessed decreased input resistance and reduced strength and duration of inhibitory inputs. In contrast, fish acclimated to 5°C were behaviorally similar to 15°C fish and had increased input resistance, increased strength of inhibitory transmission, and reduced excitatory transmission. We show here that alterations in the balance between excitatory and inhibitory synaptic transmission in the M-cell circuit underlie differences in behavioral responsiveness in acclimated populations. Specifically, during warm acclimation, synaptic inputs are weighted on the side of excitation and fish demonstrate hyperexcitability and reduced left–right discrimination during rapid escapes. In contrast, cold acclimation results in transmission weighted on the side of inhibition and these fish are less excitable and show improved directional discrimination.

Excitation of motoneurons by the Mauthner axon in goldfish: complexities in a "simple" reticulospinal pathway

1992 ◽  
Vol 67 (6) ◽  
pp. 1574-1586 ◽  
Author(s):  
J. R. Fetcho
Keyword(s):  
Escape Behavior ◽  
Mean Amplitude ◽  
Short Latency ◽  
The Body ◽  
Intracellular Recordings ◽  
M Cell ◽  
Mauthner Cell ◽  
Monosynaptic Connection ◽  
Direct Excitation ◽  
Descending Interneurons

1. The Mauthner cell in fish and amphibians initiates an escape behavior that has served as a model system for studies of the reticulospinal control of movement. This behavior consists of a very rapid bend of the body and tail that is thought to arise from the monosynaptic excitation of large primary motoneurons by the Mauthner cell. Recent work suggests that the excitation of primary motoneurons might be more complex than a solely monosynaptic connection. To examine this possibility, I used intracellular recording and staining to study the excitation of primary motoneurons by the M cell. 2. Simultaneous intracellular recordings from the M axon and ipsilateral primary motoneurons show that firing the M cell leads to complex postsynaptic potentials (PSPs) in the motoneurons. These PSPs usually have three components: an early, small, slow depolarization (component 1), a later, large, fast depolarization (component 2), and an even later, large, long-lasting depolarization (component 3). The first component has a latency of 0.52 +/- 0.15 (SD) ms, (n = 27) and most probably is a monosynaptic input from the M cell. This study focused on the two subsequent, less-understood parts of the PSP. Motoneurons typically fire off the second part of the PSP. This is usually (27 of 33 cells) the largest component, and it has a mean amplitude of 6.24 +/- 3.33 (SD) mV (n = 33) and a half-decay time of 0.44 +/- 0.18 (SD) ms (n = 27). The mean amplitude of the third component is 3.20 +/- 1.7 (SD) mV (n = 35), and its half-decay is 6.73 +/- 2.66 (SD) ms (n = 35). The latency of the second component averages 0.66 +/- 0.21 (SD) ms (n = 32), indicating that there are few synapses in the pathway mediating it. 3. One candidate pathway for the second component of the PSP involves a class of descending interneurons (DIs) that are monosynaptically, chemically excited by the M cell and appear in light microscopy to contact motoneurons. Simultaneous intracellular recordings from the M axon, a DI, and a primary motoneuron show that the interneurons are electrotonically coupled to motoneurons and produce the fast, second component of the PSP. Direct excitation of an interneuron leads to a very short-latency (less than 0.2 ms), fast PSP in a motoneuron similar to the second component of the PSP produced by the M axon. The short latency and fatigue resistance of this connection indicate it is electrotonic, and this is supported by evidence for DC coupling between the two cells.(ABSTRACT TRUNCATED AT 400 WORDS)

The Behavior of Aplysia Californica Cooper (Gastropoda; Opisthobranchia): I. Ethogram

Behaviour ◽  
1986 ◽  
Vol 98 (1-4) ◽  
pp. 320-360 ◽  
Author(s):  
Janet L. Leonard ◽  
Ken Lukowiak
Keyword(s):  
Escape Behavior ◽  
Aplysia Californica ◽  
Male Reproduction ◽  
Mechanical Stimuli ◽  
Neural Basis ◽  
Major Drawback ◽  
Motivational Systems ◽  
Sequence Of Events ◽  
Lack Of Information ◽  
Natural Predator

AbstractAplysia californica has been extremely popular with neurophysiologists interested in understanding the neural basis of behavior. The major drawback to neuroethological work on this species has been the lack of information on its behavior. We present the first ethogram of this species and a model of the physiological organization of drives (motivational systems) in Aplysia. The ethogram of A. californica contains 45 action patterns, most of which involve relatively subtle movements or postures of the head. Some of these action patterns have been studied physiologically and we summarize that information. The action patterns are superimposable and an individual may perform several action paterns simultaneously. A. californica has five distinct "drives" or motivational systems: feeding, escape, reproduction as a male, reproduction as a female and spawning. The sequence of events involved in escape behavior in response to attack by Navanax (a natural predator) or other mechanical stimuli to the rear is described. Each "drive" activates a particular sequence of action patterns, and certain "drives" are superimposable. Aplysia can copulate as a female while copulating as a male, feeding, or laying eggs. On the other hand, escape is incompatible with female sexual behavior. The available physiological evidence suggests that neuropeptides may play an important role in the organization of drives and their interactions. We present a model which combines the available physiological and behavioral data with the classical ethological drive hypothesis to produce a testable model of the physiological organization of motivation in Aplysia.

Representation of Auditory Signals in the M-Cell: Role of Electrical Synapses

2006 ◽  
Vol 95 (4) ◽  
pp. 2617-2629 ◽  
Author(s):  
T. M. Szabo ◽  
S. A. Weiss ◽  
D. S. Faber ◽  
T. Preuss
Keyword(s):  
Escape Behavior ◽  
Sensory Information ◽  
Power Spectral Analysis ◽  
Dominant Mode ◽  
M Cell ◽  
Transmission Modes ◽  
Power Spectral ◽  
Low Pass ◽  
Viiith Nerve ◽  
Lateral Dendrite

The teleost Mauthner (M-) cell mediates a sound-evoked escape behavior. A major component of the auditory input is transmitted by large myelinated club endings of the posterior VIIIth nerve. Paradoxically, although nerve stimulations revealed these afferents have mixed electrical and glutamatergic synapses on the M-cell's distal lateral dendrite, paired pre- and postsynaptic recordings indicated most individual connections are chemically silent. To determine the sensory information encoded and the relative contributions of these two transmission modes, M-cell responses to acoustic stimuli in air were recorded intracellularly. Excitatory postsynaptic potentials (EPSPs) evoked by both short 100- to 900-Hz “pips” and longer-lasting amplitude- and frequency-modulated sounds were dominated by fast, repetitive EPSPs superimposed on an underlying slow depolarization. Fast EPSPs 1) have kinetics comparable to presynaptic action potentials, 2) are maximal on the distal lateral dendrite, and 3) are insensitive to GluR antagonists. They presumably are coupling potentials, and power spectral analysis indicated they constitute a high-pass signal that accurately tracks sound frequency and amplitude. The spatial profile of the slow EPSP suggests both proximal and distal dendritic sources, a result supported by predictions of a multicompartmental model and the effects of AMPAR antagonists, which preferentially reduced the proximal component. Thus a second class of afferents generates a portion of the slow EPSP that, with sound stimuli, demonstrate that the dominant mode of transmission at LMCE synapses is electrical. The slow EPSP is a dynamic, low-pass representation of stimulus strength. Accordingly, amplitude and phase information, which are segregated in other systems, are faithfully represented in the M-cell.

Fleeing to unsafe refuges: effects of conspicuousness and refuge safety on the escape decisions of the lizard Psammodromus algirus

2000 ◽  
Vol 78 (2) ◽  
pp. 265-270 ◽  
Author(s):  
José Martín ◽  
Pilar López
Keyword(s):  
Escape Behavior ◽  
Theoretical Models ◽  
Flight Distance ◽  
Escape Performance ◽  
Lizard Species ◽  
Approach Distance ◽  
Optimal Distance ◽  
Psammodromus Algirus ◽  
Escape Decision ◽  
Escape Speed

Theoretical models of escape behavior suggest that the optimal distance at which an animal starts to flee (approach distance) increases with distance to the refuge. However, the extent of reliance on refuges may strongly affect this relationship. The lizard Psammodromus algirus escapes a predator by fleeing into leaf litter, which is very abundant but not a safe refuge because the predator could still locate and capture a concealed lizard. We test the hypothesis that escape decisions of this lizard species are based on the conspicuousness of individuals and the type of refuge used, rather than on the distance to cover per se. A field study showed that approach distance was not significantly correlated with distance to available refuges or distance actually fled. However, the type of microhabitat and the type of refuge used influenced the approach distance. Lizards started to flee earlier in microhabitats where they were presumably more visible to potential predators. Lizards ran to refuges that were similar in quality to, but farther from, the nearest available one. A longer flight may be needed to mislead the predator. However, because fleeing may be costly, the flight distance should be optimized. Thus, lizards ran farther and faster when they fled through unsafe microhabitats. Lizards with a low body temperature have lower escape performance and their approach distances should be greater. However, although air temperature affected escape speed, it was not significantly correlated with approach distance or flight distance. The relatively low reliance on refuges by P. algirus indicated that the expected relationship between escape decision and distance to the refuge did not exist. However, the results indicate that P. algirus optimizes its escape decisions according to the costs of fleeing and the costs of remaining.

Spinal Circuit for Escape in Goldfish and Zebrafish

2017 ◽  
pp. 517-520
Author(s):  
Joseph R. Fetcho
Keyword(s):  
Spinal Cord ◽  
Escape Behavior ◽  
The Body ◽  
M Cells ◽  
M Cell ◽  
Potential Threat ◽  
Reticulospinal Neurons ◽  
Bilateral Pair ◽  
The Brain ◽  
Spinal Circuit

Escape or startle responses are vital to organisms. In fishes, escape behavior is a rapid bend of the body and tail away from a potential threat that occurs within milliseconds after a stimulus. When properly executed, it is a fast, powerful body bend to only one side that takes precedence over any other movements. The behavior is initiated by the firing of one of a bilateral pair of hindbrain reticulospinal neurons (RSNs) called Mauthner cells (M-cells). The output of each cell occurs via an axon that crosses in the brain and extends the length of the spinal cord on the opposite side of the body. The circuit of the M-cell in spinal cord is based upon studies of goldfish and zebrafish. This circuit, repeated along the spinal cord, has several features that are well matched to the behavioral demands of escape movements.

Coexpression of auxiliary Kvβ2 subunits with Kv1.1 channels is required for developmental acquisition of unique firing properties of zebrafish Mauthner cells

2014 ◽  
Vol 111 (6) ◽  
pp. 1153-1164 ◽  
Author(s):  
Takaki Watanabe ◽  
Takashi Shimazaki ◽  
Aoba Mishiro ◽  
Takako Suzuki ◽  
Hiromi Hirata ◽  
...  
Keyword(s):  
Molecular Mechanisms ◽  
Escape Behavior ◽  
Repetitive Firing ◽  
M Cells ◽  
M Cell ◽  
Single Spike ◽  
Low Threshold ◽  
Firing Properties ◽  
Firing Property

Each neuron possesses a unique firing property, which is largely attributed to heterogeneity in the composition of voltage-gated ion channel complexes. Zebrafish Mauthner (M) cells, which are bilaterally paired giant reticulospinal neurons (RSNs) in the hindbrain and induce rapid escape behavior, generate only a single spike at the onset of depolarization. This single spiking is in contrast with the repetitive firing of the M cell's morphologically homologous RSNs, MiD2cm and MiD3cm, which are also involved in escapes. However, how the unique firing property of M cells is established and the underlying molecular mechanisms remain unclear. In the present study, we first demonstrated that the single-spiking property of M cells was acquired at 4 days postfertilization (dpf), accompanied by an increase in dendrotoxin I (DTX)-sensitive low-threshold K+ currents, prior to which the M cell repetitively fires as its homologs. Second, in situ hybridization showed that among DTX-sensitive Kv1 channel α-subunits, zKv1.1a was unexpectedly expressed even in the homologs and the bursting M cells at 2 dpf. In contrast, zKvβ2b, an auxiliary β-subunit of Kv1 channels, was expressed only in the single-spiking M cells. Third, zKv1.1a expressed in Xenopus oocytes functioned as a low-threshold K+ channel, and its currents were enhanced by coexpression of zKvβ2b subunits. Finally, knockdown of zKvβ2b expression in zebrafish larvae resulted in repetitive firing of M cells at 4 dpf. Taken together, these results suggest that associative expression of Kvβ2 subunits with Kv1.1 channels is crucial for developmental acquisition of the unique firing properties of the M cells among homologous neurons.

scholarly journals Correcting for physical distortions in visual stimuli improves reproducibility in zebrafish neuroscience

2019 ◽  
Author(s):  
Timothy W. Dunn ◽  
James E. Fitzgerald
Keyword(s):  
Single Neuron ◽  
Escape Behavior ◽  
Neural Mechanisms ◽  
Neuron Activity ◽  
Visually Guided ◽  
Computational Tool ◽  
Larval Zebrafish ◽  
Air Water Interface ◽  
And Control ◽  
Single Neuron Activity

Breakthrough technologies for monitoring and manipulating single-neuron activity provide unprecedented opportunities for whole-brain neuroscience in larval zebrafish1–9. Understanding the neural mechanisms of visually guided behavior also requires precise stimulus control, but little prior research has accounted for physical distortions that result from refraction and reflection at an air-water interface that usually separates the projected stimulus from the fish10–12. Here we provide a computational tool that transforms between projected and received stimuli in order to detect and control these distortions. The tool considers the most commonly encountered interface geometry, and we show that this and other common configurations produce stereotyped distortions. By correcting these distortions, we reduced discrepancies in the literature concerning stimuli that evoke escape behavior13,14, and we expect this tool will help reconcile other confusing aspects of the literature. This tool also aids experimental design, and we illustrate the dangers that uncorrected stimuli pose to receptive field mapping experiments.

scholarly journals A role of electrical inhibition in sensorimotor integration

2008 ◽  
Vol 105 (46) ◽  
pp. 18047-18052 ◽  
Author(s):  
Shennan A. Weiss ◽  
Thomas Preuss ◽  
Donald S. Faber
Keyword(s):  
Escape Behavior ◽  
Acoustic Startle ◽  
Structural Features ◽  
Cell System ◽  
M Cell ◽  
The Neural Network ◽  
Single Spike ◽  
M Spike ◽  
Cathodal Current

Although it is accepted that extracellular fields generated by neuronal activity can influence the excitability of neighboring cells, whether this form of neurotransmission has a functional role remains open. In vivo field effects occur in the teleost Mauthner (M)-cell system, where a combination of structural features support the concept of inhibitory electrical synapses. A single spike in one M-cell evoked within as little as 2.2 ms of the onset of an abrupt sound, simulating a predatory strike, initiates a startle-escape behavior [Zottoli SJ (1977) J Exp Biol 66:243–254]. We show that such sounds produce synchronized action potentials in as many as 20 or more interneurons that mediate feed-forward electrical inhibition of the M-cell. The resulting action currents produce an electrical inhibition that coincides with the electrotonic excitatory drive to the M-cell; the amplitude of the peak of the inhibition is ≈40% of that of the excitation. When electrical inhibition is neutralized with an extracellular cathodal current pulse, subthreshold auditory stimuli are converted into ones that produce an M-spike. Because the timing of electrical inhibition is often the same as the latency of M-cell firing in freely swimming fish, we conclude that electrical inhibition participates in regulating the threshold of the acoustic startle-escape behavior. Therefore, a field effect is likely to be essential to the normal functioning of the neural network.

Serotonergic modulation of startle-escape plasticity in an African cichlid fish: a single-cell molecular and physiological analysis of a vital neural circuit

2011 ◽  
Vol 106 (1) ◽  
pp. 127-137 ◽  
Author(s):  
K. W. Whitaker ◽  
H. Neumeister ◽  
L. S. Huffman ◽  
C. E. Kidd ◽  
T. Preuss ◽  
...  
Keyword(s):  
Single Cell ◽  
Social Life ◽  
Neural Circuit ◽  
Escape Behavior ◽  
Cichlid Fish ◽  
Receptor Subtype ◽  
M Cells ◽  
M Cell ◽  
Trade Off ◽  
Electrophysiological Properties

Social life affects brain function at all levels, including gene expression, neurochemical balance, and neural circuits. We have previously shown that in the cichlid fish Astatotilapia burtoni brightly colored, socially dominant (DOM) males face a trade-off between reproductive opportunities and increased predation risk. Compared with camouflaged subordinate (SUB) males, DOMs exposed to a loud sound pip display higher startle responsiveness and increased excitability of the Mauthner cell (M-cell) circuit that governs this behavior. Using behavioral tests, intracellular recordings, and single-cell molecular analysis, we show here that serotonin (5-HT) modulates this socially regulated plasticity via the 5-HT receptor subtype 2 (5-HTR2). Specifically, SUBs display increased sensitivity to pharmacological manipulation of 5-HTR2 compared with DOMs in both startle-escape behavior and electrophysiological properties of the M-cell. Immunohistochemistry showed serotonergic varicosities around the M-cells, further suggesting that 5-HT impinges directly onto the startle-escape circuitry. To determine whether the effects of 5-HTR2 are pre- or postsynaptic, and whether other 5-HTR subtypes are involved, we harvested the mRNA from single M-cells via cytoplasmic aspiration and found that 5-HTR subtypes 5A and 6 are expressed in the M-cell. 5-HTR2, however, was absent, suggesting that it affects M-cell excitability through a presynaptic mechanism. These results are consistent with a role for 5-HT in modulating startle plasticity and increase our understanding of the neural and molecular basis of a trade-off between reproduction and predation.

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