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.

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.

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.

Social and Ecological Regulation of a Decision-Making Circuit

2010 ◽  
Vol 104 (6) ◽  
pp. 3180-3188 ◽  
Author(s):  
H. Neumeister ◽  
K. W. Whitaker ◽  
H. A. Hofmann ◽  
T. Preuss
Keyword(s):  
Decision Making ◽  
Predation Risk ◽  
Neural Circuit ◽  
Physiological State ◽  
Cichlid Fish ◽  
M Cell ◽  
Body Coloration ◽  
Cryptic Coloration ◽  
Electrophysiological Recordings ◽  
Astatotilapia Burtoni

Ecological context, sensory inputs, and the internal physiological state are all factors that need to be integrated for an animal to make appropriate behavioral decisions. However, these factors have rarely been studied in the same system. In the African cichlid fish Astatotilapia burtoni, males alternate between two phenotypes based on position in a social hierarchy. When dominant (DOM), fish display bright body coloration and a wealth of aggressive and reproductive behavioral patterns that make them conspicuous to predators. Subordinate (SUB) males, on the other hand, decrease predation risk by adopting cryptic coloration and schooling behavior. We therefore hypothesized that DOMs would show enhanced startle-escape responsiveness to compensate for their increased predation risk. Indeed, behavioral responses to sound clicks of various intensities showed a significantly higher mean startle rate in DOMs compared with SUBs. Electrophysiological recordings from the Mauthner cells (M-cells), the neurons triggering startle, were performed in anesthetized animals and showed larger synaptic responses to sound clicks in DOMs, consistent with the behavioral results. In addition, the inhibitory drive mediated by interneurons (passive hyperpolarizing potential [PHP] cells) presynaptic to the M-cell was significantly reduced in DOMs. Taken together, the results suggest that the likelihood for an escape to occur for a given auditory stimulus is higher in DOMs because of a more excitable M-cell. More broadly, this study provides an integrative explanation of an ecological and social trade-off at the level of an identifiable decision-making neural circuit.

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.

Cyclic AMP Mediates Serotonin-Induced Synaptic Enhancement of Lateral Giant Interneuron of the Crayfish

2005 ◽  
Vol 94 (4) ◽  
pp. 2644-2652 ◽  
Author(s):  
Makoto Araki ◽  
Toshiki Nagayama ◽  
Jordanna Sprayberry
Keyword(s):  
Biogenic Amines ◽  
Time Course ◽  
Neural Circuit ◽  
Escape Behavior ◽  
Direct Injection ◽  
Phosphodiesterase Inhibitor ◽  
Sensory Stimulation ◽  
Simultaneous Application ◽  
Camp Analogue ◽  
Repetitive Sensory Stimulation

The lateral giant (LG)-mediated escape behavior of the crayfish habituates readily on repetitive sensory stimulation. Recent studies suggested that the biogenic amines serotonin and octopamine modulate the time course of recovery and/or re-depression of the LG response after habituation. However, little is known of how serotonin and octopamine effect LG habituation and what second-messenger cascades they may activate. To investigate the effect of biogenic amines on LG habituation, serotonin and octopamine were superfused before presenting repetitive sensory stimulation. Serotonin and octopamine increased the number of stimuli needed to habituate the LG response. Their effects were mimicked by mixed application of a cAMP analogue [8-(4-chlorophenylthio)-cAMP (CPT-cAMP)] and a phosphodiesterase inhibitor [3-isobutyl-1-methylxanthine (IBMX)] but not by a cGMP analogue (8-bromoguanosine 3′,5′-cyclic monophosphate). Perfusion of the adenylate cyclase inhibitor (SQ22536) abolished the effect of serotonin but not that of octopamine. To investigate the site of action of each biogenic amines in the neural circuit meditating LG escape, the effect of drugs on directly and indirectly elicited postsynaptic potentials in LG was investigated. Serotonin, octopamine, and a mixture of CPT-cAMP and IBMX increased both the direct and indirect synaptic inputs. Simultaneous application of SQ22536 abolished the effect of serotonin on both inputs but did not block the effect of octopamine. Direct injection of the cAMP analogue (Sp-isomer of adenosine-3′,5′-cyclic monophosphorothioate) into LG increased both the direct and indirect inputs to LG. These results indicate that serotonin mediates an increase in cAMP levels in LG, but octopamine acts independently of cAMP and cGMP.

Correlation of the startle reflex and Mauthner cell auditory responses in unrestrained goldfish

1977 ◽  
Vol 66 (1) ◽  
pp. 243-254 ◽  
Author(s):  
S. J. Zottoli
Keyword(s):  
Stainless Steel ◽  
Startle Reflex ◽  
Sound Stimulus ◽  
M Cells ◽  
M Cell ◽  
Mauthner Cell ◽  
Auditory Responses ◽  
Cell Electrode ◽  
Steel Electrodes

Stainless-steel electrodes were implanted near the left or right. Mauthner cells (M-cells) of goldfish to determine if these cells can initiate the startle reflex evoked by a brief sinusoidal sound stimulus. Recordings of the M-cell extracellular spike were obtained for the duration of 10 experiments. Fish with chronic implants were allowed to free-swim and exposed to at least 10 consecutive sound stimuli consisting of 2 cycles of 200 Hz. Seventy-three startle responses were analysed. In 34 cases the implanted M-cell electrode was contralateral to the contracting musculature, and in each of these cases, a M-cell spike preceded the EMG response by 1-1-2-1 ms. In the reamining 39 cases the electrode was ipsilateral to the active musculature, and the M-cell only fired in one of these trails. There were no startle responses and no M-cell firings in an additional 52 tests. Since the M-cell activates contralateral motoneurones, the results indicate it is responsible for initiation of the startle reflex.

Rabbit M cells and dome enterocytes are distinct cell lineages

2001 ◽  
Vol 114 (11) ◽  
pp. 2077-2083
Author(s):  
Hugues Lelouard ◽  
Alain Sahuquet ◽  
Hubert Reggio ◽  
Philippe Montcourrier
Keyword(s):  
Lymphoid Tissues ◽  
M Cells ◽  
Relative Distribution ◽  
M Cell ◽  
Epithelial Surface ◽  
Cell Lineages ◽  
Proliferative Zone ◽  
Early Appearance ◽  
Distinct Cell ◽  
Constant Distribution

We have studied the M cell origin and differentiation pathway in rabbit gut-associated lymphoid tissues. Micro-dissected domes and epithelium isolated by ethylene diamine tetra acetic acid detachment allowed us to view the whole epithelial surface from the bottom of crypts to the top of domes. We used monoclonal antibodies specific to the apex of either M cells or dome enterocytes, lectins, and antibodies to vimentin in appendix, distal Peyer’s patches and caecal patches. The earliest vimentin-labeled M cells were observed in the BrdU-positive proliferative zone of dome-associated crypts. Gradual differentiation of the M cell vimentin cytoskeleton started at this site to progressively give rise to the first pocket-forming M cells in the upper dome. Therefore, these mitotic cells of the crypts appear as the direct precursors of M cells. In addition to an early appearance of M cell markers, a regular mosaic-like relative distribution of M cells and dome enterocytes was already detected in the vicinity of crypts, similar to that observed on the lateral surface of domes where functional M cells lie. This constant distribution implies that there is no trans-differentiation of enterocytes to M cells along the crypt-dome axis. Together, these observations provide very strong evidence in favor of an early commitment in crypts of M cell and enterocyte distinct lineages.

scholarly journals Single Cell Transcriptomic Analysis of Spinal Dmrt3 Neurons in Zebrafish and Mouse Identifies Distinct Subtypes and Reveal Novel Subpopulations Within the dI6 Domain

2021 ◽  
Vol 15 ◽  
Author(s):  
Ana Belén Iglesias González ◽  
Jon E. T. Jakobsson ◽  
Jennifer Vieillard ◽  
Malin C. Lagerström ◽  
Klas Kullander ◽  
...  
Keyword(s):  
Gene Expression ◽  
Transcription Factor ◽  
Transcription Factors ◽  
Axon Guidance ◽  
Single Cell ◽  
Cellular Activity ◽  
Electrophysiological Properties ◽  
Related Transcription Factor ◽  
Unique Markers ◽  
Molecular Code

The spinal locomotor network is frequently used for studies into how neuronal circuits are formed and how cellular activity shape behavioral patterns. A population of dI6 interneurons, marked by the Doublesex and mab-3 related transcription factor 3 (Dmrt3), has been shown to participate in the coordination of locomotion and gaits in horses, mice and zebrafish. Analyses of Dmrt3 neurons based on morphology, functionality and the expression of transcription factors have identified different subtypes. Here we analyzed the transcriptomes of individual cells belonging to the Dmrt3 lineage from zebrafish and mice to unravel the molecular code that underlies their subfunctionalization. Indeed, clustering of Dmrt3 neurons based on their gene expression verified known subtypes and revealed novel populations expressing unique markers. Differences in birth order, differential expression of axon guidance genes, neurotransmitters, and their receptors, as well as genes affecting electrophysiological properties, were identified as factors likely underlying diversity. In addition, the comparison between fish and mice populations offers insights into the evolutionary driven subspecialization concomitant with the emergence of limbed locomotion.

scholarly journals CONTRAST BETWEEN THE ENVIRONMENTAL pH DEPENDENCIES OF PROPHASING AND NUCLEAR MEMBRANE FORMATION IN INTERPHASE-METAPHASE CELLS

1973 ◽  
Vol 58 (3) ◽  
pp. 608-617 ◽  
Author(s):  
Yoshitaka Obara ◽  
Hiroshi Yoshida ◽  
Lee S. Chai ◽  
Herbert Weinfeld ◽  
Avery A. Sandberg
Keyword(s):  
Structural Changes ◽  
Chinese Hamster ◽  
Binucleate Cell ◽  
M Cells ◽  
M Cell ◽  
Metaphase Chromosomes ◽  
Membrane Formation ◽  
Interphase Cell ◽  
Double Membrane ◽  
Mononucleate Cell

In Chinese hamster Don cells, fusion of an interphase cell with a metaphase cell resulted either in prophasing of the interphase nucleus, including loss of the nuclear envelope (NE), or in the formation of a double membrane around the metaphase chromosomes. Only one of these phenomena occurred in a given interphase-metaphase (I–M) binucleate cell. At pH 7.4, there was about an equal probability that either event could occur amongst the population of I–M cells. The effect of pH changes in the medium containing the fused cells was examined. At pH 6.6, prophasing was the predominant event; at pH 8.0, membrane formation predominated. It was found that the rate of progression of a mononucleate cell from G2 to metaphase was appreciably faster at pH 6.6 than at pH 8.0. Conversely, the progression from metaphase to G1 was faster at pH 8.0 than at pH 6.6. These results with the mononucleate cells strengthen the hypothesis that structural changes in I–M cells are reflections of normal mitotic phenomena. Additional evidence for this hypothesis was produced by electron microscope examination after direct fixation in chrom-osmium. The double membrane around the chromosomes of the I–M cell was indistinguishable from the normal NE. The results obtained by varying the pH of the medium containing the fused cells provide an indication that disruption or formation of the NE of Don cells depends on the balance reached between disruptive and formative processes.

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