Interaction of electrosensory and electromotor signals in lateral line lobe of a mormyrid fish

Zipser, Birgit; Bennett, M. V.L.

doi:10.1152/jn.1976.39.4.713

Cited by 78 publications

(25 citation statements)

References 0 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The slem receives input from MCA and thereby mediates corollary discharge-driven inhibition of nELL neurons (Fig.2), which blocks sensory responses for a brief window of time immediately after production of the fish's own EOD (Zipser and Bennett, 1976). The effects of this corollary discharge-driven inhibition can be seen downstream of the nELL, as stimuli delivered during a period of approximately 3ms starting immediately after the production of each EOD do not elicit electrosensory responses in the EL or KO region of the valvula (Amagai, 1998; Bennett and Steinbach, 1969;Russell and Bell, 1978;Szabo et al, 1979;Zipser and Bennett, 1976). Behavioral studies have confirmed that fish are less sensitive to electrosensory stimuli occurring up to 1.5ms after the fish's own EOD (Moller, 1970).…”

Section: Sensory Filtering and Temporal Sharpeningmentioning

confidence: 99%

“…KO afferent fibers conduct at 40ms -1 to the ipsilateral nucleus of the electrosensory lateral line lobe (nELL) in the hindbrain (Enger et al, 1976a), where corollary discharge inhibition blocks responses to the fish's own EOD (Bell and Grant, 1989;Zipser and Bennett, 1976). That is, each time an EOD motor command is generated, nELL neurons receive inhibition that prevents them from responding to sensory input.…”

Section: A Sensory Pathway Devoted To Communication Behaviormentioning

confidence: 99%

“…In addition to excitation from KO afferents, nELL cells receive GABAergic inhibitory input from the slem via small boutons that terminate on the soma and axon initial segment (Bell et al, 1981;Denizot et al, 1987;Mugnaini and Maler, 1987b;Szabo et al, 1983). The slem receives input from MCA and thereby mediates corollary discharge-driven inhibition of nELL neurons (Fig.2), which blocks sensory responses for a brief window of time immediately after production of the fish's own EOD (Zipser and Bennett, 1976). The effects of this corollary discharge-driven inhibition can be seen downstream of the nELL, as stimuli delivered during a period of approximately 3ms starting immediately after the production of each EOD do not elicit electrosensory responses in the EL or KO region of the valvula (Amagai, 1998;Bennett and Steinbach, 1969;Russell and Bell, 1978;Szabo et al, 1979;Zipser and Bennett, 1976).…”

Section: Sensory Filtering and Temporal Sharpeningmentioning

confidence: 99%

See 2 more Smart Citations

Multiplexed temporal coding of electric communication signals in mormyrid fishes

Baker

Kohashi

Lyons-Warren

et al. 2013

Journal of Experimental Biology

View full text Add to dashboard Cite

SummaryThe coding of stimulus information into patterns of spike times occurs widely in sensory systems. Determining how temporally coded information is decoded by central neurons is essential to understanding how brains process sensory stimuli. Mormyrid weakly electric fishes are experts at time coding, making them an exemplary organism for addressing this question. Mormyrids generate brief, stereotyped electric pulses. Pulse waveform carries information about sender identity, and it is encoded into submillisecond-to-millisecond differences in spike timing between receptors. Mormyrids vary the time between pulses to communicate behavioral state, and these intervals are encoded into the sequence of interspike intervals within receptors. Thus, the responses of peripheral electroreceptors establish a temporally multiplexed code for communication signals, one consisting of spike timing differences between receptors and a second consisting of interspike intervals within receptors. These signals are processed in a dedicated sensory pathway, and recent studies have shed light on the mechanisms by which central circuits can extract behaviorally relevant information from multiplexed temporal codes. Evolutionary change in the anatomy of this pathway is related to differences in electrosensory perception, which appears to have influenced the diversification of electric signals and species. However, it remains unknown how this evolutionary change relates to differences in sensory coding schemes, neuronal circuitry and central sensory processing. The mormyrid electric communication pathway is a powerful model for integrating mechanistic studies of temporal coding with evolutionary studies of correlated differences in brain and behavior to investigate neural mechanisms for processing temporal codes.Key words: sub-millisecond timing differences, duration tuning, interval tuning, coincidence detection, anti-coincidence detection, delay line, temporal filter, weakly electric fish, electric organ discharge. Division of Biological Science, Graduate School of Science, Nagoya University, Nagoya, Japan *Author for correspondence (carlson.bruce@wustl.edu) THE JOURNAL OF EXPERIMENTAL BIOLOGY 2366 that links changes in neural circuitry to differences in behavior. From the perspective of the central nervous system, there is no difference between the electrosense and other modalities -all stimuli are represented as patterns of spiking. Therefore, the mechanisms by which mormyrids process temporally coded information are relevant to understanding basic principles for how any neural circuit can solve this problem.Electric signals in mormyrid fishes communicate sender identity and behavioral state Two components of electrocommunication: EOD and IPI Mormyrids produce an electric organ discharge (EOD) to communicate and actively sense their environment (Hopkins, 1986). These fish have three types of electroreceptors in their skin: mormyromasts are used for active sensing, ampullary receptors for passive sensing and knollenorgans for commun...

show abstract

Section: Sensory Filtering and Temporal Sharpeningmentioning

confidence: 99%

Section: A Sensory Pathway Devoted To Communication Behaviormentioning

confidence: 99%

Section: Sensory Filtering and Temporal Sharpeningmentioning

confidence: 99%

See 1 more Smart Citation

Multiplexed temporal coding of electric communication signals in mormyrid fishes

Baker

Kohashi

Lyons-Warren

et al. 2013

Journal of Experimental Biology

View full text Add to dashboard Cite

show abstract

“…The Knollenorgan pathway is briefly inhibited each time a fish fires its own electric organ, resulting in a selective responsiveness to EODs produced by other individuals rather than to selfgenerated EODs (Zipser and Bennett, 1976;Mugnaini and Maler, 1987;Bell and Grant, 1989). Knollenorgan cells fire spike-like receptor potentials that are time locked to outside negative-to-positive (NrP) voltage transients (Bennett, 1971b;Szabo and Fessard, 1974).…”

Section: Introductionmentioning

confidence: 99%

Time-domain signal divergence and discrimination without receptor modification in sympatric morphs of electric fishes

Arnegard

Jackson

Hopkins

2006

Journal of Experimental Biology

View full text Add to dashboard Cite

SUMMARY Polymorphism in an animal communication channel provides a framework for studying proximate rules of signal design as well as ultimate mechanisms of signal diversification. Reproductively isolated mormyrid fishes from Gabon's Brienomyrus species flock emit distinctive electric organ discharges(EODs) thought to function in species and sex recognition. Species boundaries and EODs appear congruent in these fishes, with the notable exception of three morphs designated types I, II and III. Within the species flock, these morphs compose a monophyletic group that has recently been called the magnostipes complex. Co-occurring morphs of this complex express distinctive EODs, yet they appear genetically indistinguishable at several nuclear loci. In this study, we investigated EOD discrimination by these morphs using both behavioral and physiological experiments. During the breeding season, wild-caught type I and type II males showed evidence that they can discriminate their own morph's EOD waveform from that of a sympatric and genetically distinct reference species. However, we found that type I and type II males exhibited an asymmetry in unconditioned responses to paired playback of EODs recorded from type I versus type II females. Males of the type II morph responded preferentially to EODs of type II females,whereas type I males did not appear to discriminate homotypic and heterotypic EODs in our experimental paradigm. Part of this behavioral asymmetry may have resulted from a previously undetected difference in adult size, which may have enhanced apparent discrimination by the smaller morph (type II) due to a relatively higher risk of injury from the larger morph (type I). Knollenorgan receptors, which mediate electrical communication in mormyrids, showed similar spectral tuning in type I and type II. These electroreceptors coded temporal features of any single magnostipes-complex EOD with similar patterns of time-locked spikes in both morphs. By contrast, Knollenorgans exhibited distinctive responses to different EOD waveforms. These results suggest that discrete EOD variation in this rapidly diversifying complex is functional in terms of morph-specific advertisement and recognition. Time-domain signal divergence has outpaced frequency-domain divergence between sympatric morphs,requiring little to no change in receptor response properties. We discuss our findings in light of a model for EOD time-coding by the Knollenorgan pathway,as well as evolutionary hypotheses concerning sympatric signal diversification in the magnostipes complex.

show abstract

“…With each EOD, the electrosensory lobe receives both reafferent input and corollary discharge input associated with the motor command that elicits the EOD (11,12). The corollary discharge input arises from three or four different central sources (8,9,13), and the effects are both excitatory and inhibitory (7,8).…”

mentioning

confidence: 99%

Storage of a sensory pattern by anti-Hebbian synaptic plasticity in an electric fish.

Bell

Caputi

Grant

et al. 1993

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

111

View full text Add to dashboard Cite

Synaptic plasticity occurs in several regions of the vertebrate brain and is believed to mediate the storage of behaviorally significant information during learning. Synaptic plasticity is well demonstrated in most cases, but the behavioral meaning of the relevant neural signals and the behavioral role of the plasticity are uncertain. In this paper we describe a case of synaptic plasticity which involves identifiable sensory and motor signals and which appears to mediate the storage of an image of past sensory input. Corollary discharge signals associated with the motor command that drives the electric organ are prominent in the electrosensory lobe of mormyrid electric fish. Some of these corollary discharge signals elicit a negative image or representation of the electrosensory input pattern that has followed recent motor commands. When the temporal and spatial pattern of sensory input changes, the corollary discharge effect also changes in a corresponding manner. The cellular mechanisms by which the corollary discharge-evoked representation is stored were investigated by intracellular recording from cells of the electrosensory lobe and pairing intracellular current pulses with the corollary discharge signal. The results indicate that the representation of recent sensory input is stored by means of anti-Hebbian plasticity at the synapses between corollary discharge-conveying fibers and cells of the electrosensory lobe. The results also suggest that dendritic spikes and plasticity at inhibitory synapses are involved in the phenomenon.Many sensory regions of the brain are affected by signals of central origin that are associated with motor commands (1-3). These signals are known as efference copy (4) or corollary discharge (5) signals and prepare the sensory regions for the (re)afferent (4) input that follows a commanded motor action. Optimal interaction between reafferent and corollary discharge inputs requires an approximate match in the timing and spatial distribution of the two signals. This requirement for matching, and the likelihood of variation in reafferent input, suggests that some corollary discharge effects may be plastic. Plastic corollary discharge effects are in fact present in the mormyrid electrosensory lobe (6-8).The electrosensory lobe is the termination site for afferent fibers from the three classes of electroreceptors in mormyrid fish: knollenorgans, ampullary organs, and mormyromasts (9). This paper is concerned only with the regions that receive ampullary and mormyromast input. Ampullary afferents project to the ventrolateral zone of the electrosensory lobe cortex, and mormyromast afferents project to the medial and dorsolateral zones (Fig. 1A). The projections are somatotopically organized. The histological structure of the cortex is like that of the cerebellum and contains Purkinje-like cells (9, 10) with cell bodies in the deeper layers and apical dendrites in the molecular layer.Each electric organ discharge (EOD) evokes reafferent responses in ampullary and mormyromast fibers ...

show abstract

Interaction of electrosensory and electromotor signals in lateral line lobe of a mormyrid fish

Cited by 78 publications

References 0 publications

Multiplexed temporal coding of electric communication signals in mormyrid fishes

Multiplexed temporal coding of electric communication signals in mormyrid fishes

Time-domain signal divergence and discrimination without receptor modification in sympatric morphs of electric fishes

Storage of a sensory pattern by anti-Hebbian synaptic plasticity in an electric fish.

Contact Info

Product

Resources

About