Physiology and ultrastructure of electrotonic junctions. II. Spinal and medullary electromotor nuclei in mormyrid fish.

Bennett, M. V.L.; Pappas, George D.; Aljure, E.; Nakajima, Yoshiaki

doi:10.1152/jn.1967.30.2.180

Cited by 149 publications

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“…The increase in action potential duration that we have recorded is unlikely to be use dependent, since both treated and untreated fish produce EODs that are used in continuously ongoing orientation and communication behaviors (7,8). It still remains possible that there are changes in the rate or frequency at which an EOD is generated (i.e., the EOD rhythm), which would be under central control (16). However, several lines of evidence, together with the present study, indicate that steroids exert their effects on the EOD pulse waveform by directly changing the anatomy and physiology of the electrocytes rather than components of the central ele'ctromotor pathway.…”

Section: Discussionmentioning

confidence: 88%

“…1C) and is innervated by spinal "electromotoneurons." A descending signal from the brain synchronously activates the motoneurons, which in turn synchronously activate all of the electrocytes (16). The sequential action potentials generated by the posterior and then the anterior faces of a single electrocyte determine the appearance of, respectively, the major head-positive and head-negative phases of an EOD, while the stalk determines an initial head negativity in species whose stalk penetrates through the electrocyte body (6,15) ( Fig.…”

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confidence: 99%

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From behavior to membranes: testosterone-induced changes in action potential duration in electric organs.

Bass

Volman

1987

Proc. Natl. Acad. Sci. U.S.A.

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The electric organ of mormyrid fishes consists of action potential-generating cells called electrocytes, which together produce a pulse-like electric organ discharge (EOD). The appearance of an EOD depends, in part, on the characteristic features of a single electrocyte's action potentials. In some species, gonadal steroid hormones induce increases in EOD duration, which mimic natural sex differences. We now show that testosterone-induced changes in EOD duration are associated with a 2-to 3-fold increase in the duration of action potentials generated by single electrocytes.Together with other anatomical and biochemical data, the results emphasize the exquisite interrelationship between steroid hormone action and the cellular machinery determining the electrical properties of single cells that underlie sexually dimorphic and seasonal behaviors.Among many vertebrates, the development and evolution of sex differences in social communication systems has been linked with the potent effects of gonadal steroid hormones on neurons and muscles (1-5). This includes the electrogenic system of the mormyrid fishes of Africa, which have an electric organ consisting of modified muscle cells called electrocytes (6) that generate an electric organ discharge (EOD) used in social communication and guidance systems (7,8). The EOD is a unique behavior because it is also a discrete spike-like event whose principal features are determined by a single electrocyte (6). In several species, the EOD is sexually dimorphic and the male pulse may be 2-3 times the duration of the female's during the breeding season (8-12); gonadal steroid hormones can induce females to generate a male-like EOD (4, 12).The mormyrid electric organ is located in the tail (Fig. 1A) and consists of four columns of electrocytes, which are wafer-shaped cells with distinct anterior and posterior faces ( Fig. 1 B and C) (6,(13)(14)(15). Each electrocyte also has a "stalk" system that arises from the posterior face (Fig. 1C) and is innervated by spinal "electromotoneurons." A descending signal from the brain synchronously activates the motoneurons, which in turn synchronously activate all of the electrocytes (16). The sequential action potentials generated by the posterior and then the anterior faces of a single electrocyte determine the appearance of, respectively, the major head-positive and head-negative phases of an EOD, while the stalk determines an initial head negativity in species whose stalk penetrates through the electrocyte body (6, 15) ( Fig. 1 C and D).Using intracellular recording techniques, we have now found that the effects of gonadal steroids on EOD duration, a sexually dimorphic feature in mormyrid electric fish, is correlated with comparable changes in the duration of action potentials generated by single electrocytes. The results exemplify how steroid hormones can ultimately influence the induction of different behaviors by orchestrating changes in the fundamental events that determine the electrical and anatomical properties of individual c...

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Section: Discussionmentioning

confidence: 88%

mentioning

confidence: 99%

From behavior to membranes: testosterone-induced changes in action potential duration in electric organs.

Bass

Volman

1987

Proc. Natl. Acad. Sci. U.S.A.

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“…Although the electric organ is silenced by flaxedil, the EOD command can be recorded as a three-spike potential resulting from the synchronous activation of EMN (Bennett et al, 1967). The first negative peak in the EMN volley was defined as the reference time for EOD output (t0), which in a natural situation precedes the EOD by 4-5·ms.…”

Section: Methodsmentioning

confidence: 99%

Central control of electric signaling behavior in the mormyridBrienomyrus brachyistius: segregation of behavior-specific inputs and the role of modifiable recurrent inhibition

Carlson

Hopkins

2004

Journal of Experimental Biology

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SUMMARY Like all mormyrid fish, Brienomyrus brachyistius produces an electric organ discharge (EOD) with a constant waveform and variable sequence of pulse intervals (SPI). Periodic bursts fall into two display categories termed `scallops' and `accelerations', with a third category termed `rasps'that appears to combine the two. The medullary EOD command nucleus (CN)receives excitatory input from the midbrain precommand nucleus (PCN) and the thalamic dorsal posterior nucleus (DP), both of which are regulated by a recurrent inhibitory projection from the ventroposterior nucleus of the torus semicircularis (VP). We tested the following hypotheses: (1) PCN and DP are responsible for generating different burst types (scallops and accelerations,respectively), (2) differences in the strength of recurrent inhibition are related to physiological differences between PCN and DP and (3) recurrent inhibition regulates the resting electromotor rhythm, while disinhibition releases PCN and DP, allowing them to generate bursts. Iontophoresis of the excitatory neurotransmitter l-glutamate (l-Glu) into DP led to acceleration-like output patterns, while in PCN it led to scallop-like output patterns. Iontophoresis of the inhibitory neurotransmitterγ-amino-butyric acid (GABA) into DP and PCN led to an elongation of intervals, as did iontophoresis of l-Glu into VP. Iontophoresis of the GABAA receptor blocker bicuculline methiodide (BMI) into DP and PCN induced repetitive bursting behavior and eliminated differences in the effects of l-Glu iontophoresis in the two nuclei. These results support our three hypotheses, suggesting that production of different communication behaviors may be regulated by spatially distinct groups of neurons, and recurrent inhibition and disinhibition may play an active role in driving and shaping such behaviors.

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“…The older literature has long contained data which suggested that the ability to con trol firing patterns was a fundamental capa bility of at least certain neurons. For example, figure 9 shows an example from fish motor system wherein the threshold response is not one spike but two [56]. Here are photographi cally superimposed traces of the responses to a depolarizing current adjusted to be just at spike threshold.…”

Section: Creating Temporal Structures In Neuronsmentioning

confidence: 99%

“…Patterning of synchronous spike discharges at threshold in two electrically coupled fish motor neu rons [56). Simultaneous intracellular recordings from both neurons yield the two upper sets of photographi cally superimposed traces.…”

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confidence: 99%

Isomorphism, Task Dependence, and the Multiple Meaning Theory of Neural Coding (Part 2 of 2)

Wasserman¹

1992

Neurosignals

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The neural coding problem is defined and several possible answers to it are reviewed. A widely accepted answer descends from early suggestions that neural activity, in general, is isomorphic with sensation and that the biological signals resident in the axons of neurons, in particular, are given by their frequency of firing. More recent data are reviewed which indicate that the pattern of neural responses may also be informative. Such data led to the formulation of the multiple meaning theory which suggests the neural pattern may encode different information features in single responses. After a period in which attention turned elsewhere, the multiple meaning theory has quite recently been revived and has stimulated novel and careful experimental investigations. A corollary theory, the task dependence hypothesis, suggests that these information-bearing multiple response features are accessed differentially in different behavioral tasks. These theories place stringent temporal requirements on the generation and analysis of neural responses. Recent data are examined indicating that both requirements may indeed be satisfied by the nervous system. Finally, several methods of experimentally testing such coding theories are described; they involve manipulating the biological signals of neurons and observing the effect of these manipulations on behavior.

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Physiology and ultrastructure of electrotonic junctions. II. Spinal and medullary electromotor nuclei in mormyrid fish.

Cited by 149 publications

References 0 publications

From behavior to membranes: testosterone-induced changes in action potential duration in electric organs.

From behavior to membranes: testosterone-induced changes in action potential duration in electric organs.

Central control of electric signaling behavior in the mormyridBrienomyrus brachyistius: segregation of behavior-specific inputs and the role of modifiable recurrent inhibition

Isomorphism, Task Dependence, and the Multiple Meaning Theory of Neural Coding (Part 2 of 2)

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