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Frank Kirschbaum - One of the best experts on this subject based on the ideXlab platform.
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evidence for mutual allocation of social attention through interactive signaling in a Mormyrid weakly electric fish
Proceedings of the National Academy of Sciences of the United States of America, 2018Co-Authors: Martin Worm, Tim Landgraf, Julia Prume, Frank Kirschbaum, Hai Nguyen, Gerhard Von Der EmdeAbstract:Mormyrid weakly electric fish produce electric organ discharges (EODs) for active electrolocation and electrocommunication. These pulses are emitted with variable interdischarge intervals (IDIs) resulting in temporal discharge patterns and interactive signaling episodes with nearby conspecifics. However, unequivocal assignment of interactive signaling to a specific behavioral context has proven to be challenging. Using an ethorobotical approach, we confronted single individuals of weakly electric Mormyrus rume proboscirostris with a mobile fish robot capable of interacting both physically, on arbitrary trajectories, as well as electrically, by generating echo responses through playback of species-specific EODs, thus synchronizing signals with the fish. Interactive signaling by the fish was more pronounced in response to a dynamic echo playback generated by the robot than in response to playback of static random IDI sequences. Such synchronizations were particularly strong at a distance corresponding to the outer limit of active electrolocation, and when fish oriented toward the fish replica. We therefore argue that interactive signaling through echoing of a conspecific’s EODs provides a simple mechanism by which weakly electric fish can specifically address nearby individuals during electrocommunication. Echoing may thus enable Mormyrids to mutually allocate social attention and constitute a foundation for complex social behavior and relatively advanced cognitive abilities in a basal vertebrate lineage.
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social interactions between live and artificial weakly electric fish electrocommunication and locomotor behavior of mormyrus rume proboscirostris towards a mobile dummy fish
PLOS ONE, 2017Co-Authors: Martin Worm, Frank Kirschbaum, Gerhard Von Der EmdeAbstract:Mormyrid weakly electric fish produce short, pulse-type electric organ discharges for actively probing their environment and to communicate with conspecifics. Animals emit sequences of pulse-trains that vary in overall frequency and temporal patterning and can lead to time-locked interactions with the discharge activity of other individuals. Both active electrolocation and electrocommunication are additionally accompanied by stereotypical locomotor patterns. However, the concrete roles of electrical and locomotor patterns during social interactions in Mormyrids are not well understood. Here we used a mobile fish dummy that was emitting different types of electrical playback sequences to study following behavior and interaction patterns (electrical and locomotor) between individuals of weakly electric fish. We confronted single individuals of Mormyrus rume proboscirostris with a mobile dummy fish designed to attract fish from a shelter and recruit them into an open area by emitting electrical playbacks of natural discharge sequences. We found that fish were reliably recruited by the mobile dummy if it emitted electrical signals and followed it largely independently of the presented playback patterns. While following the dummy, fish interacted with it spatially by displaying stereotypical motor patterns, as well as electrically, e.g. through discharge regularizations and by synchronizing their own discharge activity to the playback. However, the overall emission frequencies of the dummy were not adopted by the following fish. Instead, social signals based on different temporal patterns were emitted depending on the type of playback. In particular, double pulses were displayed in response to electrical signaling of the dummy and their expression was positively correlated with an animals' rank in the dominance hierarchy. Based on additional analysis of swimming trajectories and stereotypical locomotor behavior patterns, we conclude that the reception and emission of electrical communication signals play a crucial role in mediating social interactions in Mormyrid weakly electric fish.
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Electric organ discharge diversification in Mormyrid weakly electric fish is associated with differential expression of voltage-gated ion channel genes
Journal of Comparative Physiology A, 2017Co-Authors: Rebecca Nagel, Frank Kirschbaum, Ralph TiedemannAbstract:In Mormyrid weakly electric fish, the electric organ discharge (EOD) is used for species recognition, orientation and prey localization. Produced in the muscle-derived adult electric organ, the EOD exhibits a wide diversity across species in both waveform and duration. While certain defining EOD characteristics can be linked to anatomical features of the electric organ, many factors underlying EOD differentiation are yet unknown. Here, we report the differential expression of 13 Kv1 voltage-gated potassium channel genes, two inwardly rectifying potassium channel genes, two previously studied sodium channel genes and an ATPase pump in two sympatric species of the genus Campylomormyrus in both the adult electric organ and skeletal muscle. Campylomormyrus compressirostris displays a basal EOD, largely unchanged during development, while C. tshokwe has an elongated, putatively derived discharge. We report an upregulation in all Kv1 genes in the electric organ of Campylomormyrus tshokwe when compared to both skeletal muscle and C. compressirostris electric organ. This pattern of upregulation in a species with a derived EOD form suggests that voltage-gated potassium channels are potentially involved in the diversification of the EOD signal among Mormyrid weakly electric fish.
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Evidence for Non-neutral Evolution in a Sodium Channel Gene in African Weakly Electric Fish (Campylomormyrus, Mormyridae)
Journal of Molecular Evolution, 2016Co-Authors: Christiane Paul, Victor Mamonekene, Frank Kirschbaum, Ralph TiedemannAbstract:Voltage-gated sodium channels, Nav1, play a crucial role in the generation and propagation of action potentials and substantially contribute to the shape of their rising phase. The electric organ discharge (EOD) of African weakly electric fish (Mormyroidea) is the sum of action potentials fired from all electrocytes of the electric organ at the same time and hence voltage-gated sodium channels are one factor—together with the electrocyte’s morphology and innervation pattern—that determines the properties of these EODs. Due to the fish-specific genome duplication, teleost fish possess eight copies of sodium channel genes (SCN), which encode for Nav1 channels. In mormyroids, SCN4aa is solely expressed in the electrocytes of the adult electric organ. In this study, we compared entire SCN4aa sequences of six species of the genus Campylomormyrus and identified nonsynonymous substitutions among them. SCN4aa in Campylomormyrus exhibits a much higher evolutionary rate compared to its paralog SCN4ab, whose expression is not restricted to the electric organ. We also found evidence for strong positive selection on the SCN4aa gene within Mormyridae and along the lineage ancestral to the Mormyridae. We have identified sites at which all nonelectric teleosts are monomorphic in their amino acid, but Mormyrids have different amino acids. Our findings confirm the crucial role of SCN4aa in EOD evolution among Mormyrid weakly electric fish. The inferred positive selection within Mormyridae makes this gene a prime candidate for further investigation of the divergent evolution of pulse-type EODs among closely related species.
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Comparative histology of the adult electric organ among four species of the genus Campylomormyrus (Teleostei: Mormyridae)
Journal of Comparative Physiology A, 2015Co-Authors: Christiane Paul, Jacob Engelmann, Philine G D Feulner, Victor Mamonekene, Ralph Tiedemann, Marianne Vater, Frank KirschbaumAbstract:The electric organ (EO) of weakly electric Mormyrids consists of flat, disk-shaped electrocytes with distinct anterior and posterior faces. There are multiple species-characteristic patterns in the geometry of the electrocytes and their innervation. To further correlate electric organ discharge (EOD) with EO anatomy, we examined four species of the Mormyrid genus Campylomormyrus possessing clearly distinct EODs. In C. compressirostris , C. numenius , and C. tshokwe , all of which display biphasic EODs, the posterior face of the electrocytes forms evaginations merging to a stalk system receiving the innervation. In C. tamandua that emits a triphasic EOD, the small stalks of the electrocyte penetrate the electrocyte anteriorly before merging on the anterior side to receive the innervation. Additional differences in electrocyte anatomy among the former three species with the same EO geometry could be associated with further characteristics of their EODs. Furthermore, in C. numenius , ontogenetic changes in EO anatomy correlate with profound changes in the EOD. In the juvenile the anterior face of the electrocyte is smooth, whereas in the adult it exhibits pronounced surface foldings. This anatomical difference, together with disparities in the degree of stalk furcation, probably contributes to the about 12 times longer EOD in the adult.
Ralph Tiedemann - One of the best experts on this subject based on the ideXlab platform.
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Electric organ discharge diversification in Mormyrid weakly electric fish is associated with differential expression of voltage-gated ion channel genes
Journal of Comparative Physiology A, 2017Co-Authors: Rebecca Nagel, Frank Kirschbaum, Ralph TiedemannAbstract:In Mormyrid weakly electric fish, the electric organ discharge (EOD) is used for species recognition, orientation and prey localization. Produced in the muscle-derived adult electric organ, the EOD exhibits a wide diversity across species in both waveform and duration. While certain defining EOD characteristics can be linked to anatomical features of the electric organ, many factors underlying EOD differentiation are yet unknown. Here, we report the differential expression of 13 Kv1 voltage-gated potassium channel genes, two inwardly rectifying potassium channel genes, two previously studied sodium channel genes and an ATPase pump in two sympatric species of the genus Campylomormyrus in both the adult electric organ and skeletal muscle. Campylomormyrus compressirostris displays a basal EOD, largely unchanged during development, while C. tshokwe has an elongated, putatively derived discharge. We report an upregulation in all Kv1 genes in the electric organ of Campylomormyrus tshokwe when compared to both skeletal muscle and C. compressirostris electric organ. This pattern of upregulation in a species with a derived EOD form suggests that voltage-gated potassium channels are potentially involved in the diversification of the EOD signal among Mormyrid weakly electric fish.
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Evidence for Non-neutral Evolution in a Sodium Channel Gene in African Weakly Electric Fish (Campylomormyrus, Mormyridae)
Journal of Molecular Evolution, 2016Co-Authors: Christiane Paul, Victor Mamonekene, Frank Kirschbaum, Ralph TiedemannAbstract:Voltage-gated sodium channels, Nav1, play a crucial role in the generation and propagation of action potentials and substantially contribute to the shape of their rising phase. The electric organ discharge (EOD) of African weakly electric fish (Mormyroidea) is the sum of action potentials fired from all electrocytes of the electric organ at the same time and hence voltage-gated sodium channels are one factor—together with the electrocyte’s morphology and innervation pattern—that determines the properties of these EODs. Due to the fish-specific genome duplication, teleost fish possess eight copies of sodium channel genes (SCN), which encode for Nav1 channels. In mormyroids, SCN4aa is solely expressed in the electrocytes of the adult electric organ. In this study, we compared entire SCN4aa sequences of six species of the genus Campylomormyrus and identified nonsynonymous substitutions among them. SCN4aa in Campylomormyrus exhibits a much higher evolutionary rate compared to its paralog SCN4ab, whose expression is not restricted to the electric organ. We also found evidence for strong positive selection on the SCN4aa gene within Mormyridae and along the lineage ancestral to the Mormyridae. We have identified sites at which all nonelectric teleosts are monomorphic in their amino acid, but Mormyrids have different amino acids. Our findings confirm the crucial role of SCN4aa in EOD evolution among Mormyrid weakly electric fish. The inferred positive selection within Mormyridae makes this gene a prime candidate for further investigation of the divergent evolution of pulse-type EODs among closely related species.
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Comparative histology of the adult electric organ among four species of the genus Campylomormyrus (Teleostei: Mormyridae)
Journal of Comparative Physiology A, 2015Co-Authors: Christiane Paul, Jacob Engelmann, Philine G D Feulner, Victor Mamonekene, Ralph Tiedemann, Marianne Vater, Frank KirschbaumAbstract:The electric organ (EO) of weakly electric Mormyrids consists of flat, disk-shaped electrocytes with distinct anterior and posterior faces. There are multiple species-characteristic patterns in the geometry of the electrocytes and their innervation. To further correlate electric organ discharge (EOD) with EO anatomy, we examined four species of the Mormyrid genus Campylomormyrus possessing clearly distinct EODs. In C. compressirostris , C. numenius , and C. tshokwe , all of which display biphasic EODs, the posterior face of the electrocytes forms evaginations merging to a stalk system receiving the innervation. In C. tamandua that emits a triphasic EOD, the small stalks of the electrocyte penetrate the electrocyte anteriorly before merging on the anterior side to receive the innervation. Additional differences in electrocyte anatomy among the former three species with the same EO geometry could be associated with further characteristics of their EODs. Furthermore, in C. numenius , ontogenetic changes in EO anatomy correlate with profound changes in the EOD. In the juvenile the anterior face of the electrocyte is smooth, whereas in the adult it exhibits pronounced surface foldings. This anatomical difference, together with disparities in the degree of stalk furcation, probably contributes to the about 12 times longer EOD in the adult.
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magic trait electric organ discharge eod dual function of electric signals promotes speciation in african weakly electric fish
Communicative & Integrative Biology, 2009Co-Authors: Philine G D Feulner, Jacob Engelmann, Frank Kirschbaum, Martin Plath, Ralph TiedemannAbstract:A unique evolutionary specialization of African weakly electric fish (Mormyridae) is their ability to produce and perceive electric signals. Mormyrids use their Electric Organs Discharge (EOD) for electrolocation and electrocommunication. Here we discuss the adaptive significance of the EOD in foraging (electric prey detection) in light of recent results demonstrating that Mormyrid fish mate assortatively according to EOD waveform characteristics (electric mate choice). Therefore the EOD as a single trait pleiotropically combines natural divergent selection and reproductive isolation. Consequently we postulate the EOD as a “magic trait” promoting the diversification of African weakly electric fish.
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magic trait electric organ discharge eod dual function of electric signals promotes speciation in african weakly electric fish
Communicative & Integrative Biology, 2009Co-Authors: Philine G D Feulner, Jacob Engelmann, Frank Kirschbaum, Martin Plath, Ralph TiedemannAbstract:A unique evolutionary specialization of African weakly electric fish (Mormyridae) is their ability to produce and perceive electric signals. Mormyrids use their Electric Organs Discharge (EOD) for electrolocation and electrocommunication. Here we discuss the adaptive significance of the EOD in foraging (electric prey detection) in light of recent results demonstrating that Mormyrid fish mate assortatively according to EOD waveform characteristics (electric mate choice). Therefore the EOD as a single trait pleiotropically combines natural divergent selection and reproductive isolation. Consequently we postulate the EOD as a “magic trait” promoting the diversification of African weakly electric fish.
Curtis C Bell - One of the best experts on this subject based on the ideXlab platform.
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synaptic plasticity and calcium signaling in purkinje cells of the central cerebellar lobes of Mormyrid fish
The Journal of Neuroscience, 2007Co-Authors: Victor Z Han, Curtis C Bell, Yueping Zhang, Christian HanselAbstract:Climbing fiber (CF)-evoked calcium transients play a key role in plasticity at parallel fiber (PF) to Purkinje cell synapses in the mammalian cerebellum. Whereas PF activation alone causes long-term potentiation (LTP), coactivation of the heterosynaptic CF input, which evokes large dendritic calcium transients, induces long-term depression (LTD). This unique type of heterosynaptic interaction is a hallmark feature of synaptic plasticity in mammalian Purkinje cells. Purkinje cells in the cerebellum of Mormyrid electric fish are characterized by a different architecture of their dendritic trees and by a more pronounced separation of CF and PF synaptic contact sites. We therefore examined the conditions for bidirectional plasticity at PF synapses onto Purkinje cells in the Mormyrid cerebellum in vitro. PF stimulation at elevated frequencies induces LTP, whereas LTD results from PF stimulation at enhanced intensities and depends on dendritic calcium influx and metabotropic glutamate receptor type 1 activation. LTD can also be observed after pairing of low intensity PF stimulation with CF stimulation. Using a combination of whole-cell patch-clamp recordings and fluorometric calcium imaging, we characterized calcium transients in Purkinje cell dendrites. CF activation elicits calcium transients not only within the CF input territory (smooth proximal dendrites) but also within the PF input territory (spiny palisade dendrites). Paired PF and CF activation elicits larger calcium transients than stimulation of either input alone. A major source for dendritic calcium signaling is provided by P/Q-type calcium channels. Our data show that despite the spatial separation between the two inputs CF activity facilitates LTD induction at PF synapses.
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anatomy of the posterior caudal lobe of the cerebellum and the eminentia granularis posterior in a Mormyrid fish
The Journal of Comparative Neurology, 2007Co-Authors: Holly R Campbell, Jianmei Zhang, J Meek, Curtis C BellAbstract:The cerebellum of Mormyrid fish is of interest for its large size and unusual histology. The Mormyrid cerebellum, as in all ray-finned fishes, has three subdivisions--valvula, corpus, and caudal lobe. The structures of the Mormyrid valvula and corpus have been examined previously, but the structure of the Mormyrid caudal lobe has not been studied. The Mormyrid caudal lobe includes a posterior caudal lobe associated with the electrosense and an anterior caudal lobe associated with lateral line and eighth nerve senses. In this article we describe cellular elements of the posterior caudal lobe and of the eminentia granularis posterior (EGp) in the Mormyrid fish Gnathonemus petersii. The EGp gives rise to the parallel fibers of the posterior caudal lobe. We used intracellular injection of biocytin, extracellular injection of biotinylated dextran amine, and immunohistochemistry with antibodies to gamma-aminobutyric acid, inositol triphosphate receptor I, calretinin, and Zebrin II. The histological structure of the posterior caudal lobe is markedly irregular in comparison to that of the corpus and the valvula, and a tight modular organization of cerebellar elements is less apparent here. Most Purkinje cell bodies are in the middle of the molecular region. Their dendrites are only roughly oriented in the sagittal plane, extend both ventrally and dorsally, and branch irregularly. Climbing fibers terminate only on smooth dendrites near the soma. Most Purkinje cell axons terminate locally on eurydendroid cells that project outside the cortex. The results provide an additional variant to the already large set of different cerebellar and cerebellum-like structures.
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granular cells of the Mormyrid electrosensory lobe and postsynaptic control over presynaptic spike occurrence and amplitude through an electrical synapse
Journal of Neurophysiology, 2007Co-Authors: Jianmei Zhang, Victor Z Han, J Meek, Curtis C BellAbstract:Primary afferent fibers from the electroreceptors of Mormyrid electric fish use a latency code to signal the intensity of electrical current evoked by the fish's own electric organ discharge (EOD)....
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cell morphology and circuitry in the central lobes of the Mormyrid cerebellum
The Journal of Comparative Neurology, 2006Co-Authors: Victor Z Han, J Meek, Holly R Campbell, Curtis C BellAbstract:The cerebellum of Mormyrid electric fish is large and unusually regular in its histological structure. We have examined the morphology of cellular elements in the central lobes of the Mormyrid cerebellum. We have used intracellular injection of biocytin to determine the morphology of cells with somas in the cortex, and we have used extracellular placement of anterograde tracers in the inferior olive to label climbing fibers. Our results confirm previous Golgi studies and extend them by providing a more complete description of axonal trajectories. Most Purkinje cells in Mormyrids and other actinopterygian fishes are interneurons that terminate locally in the cortex on efferent neurons that are equivalent to cerebellar nucleus cells in mammals. We confirm the markedly sagittal distribution of the fan-like dendrites of Purkinje cells, efferent cells, and molecular layer interneurons. We show that Purkinje cell axons extend further than was previously thought in the sagittal plane. We show that climbing fibers are distributed in narrow sagittal strips and that these fibers terminate exclusively in the ganglionic layer below the molecular layer where parallel fibers terminate. Our results together with those of others show that the central lobes of the Mormyrid cerebellum, similar to the mammalian cerebellum, are composed of sagittally oriented modules made up of Purkinje cells, climbing fibers, molecular layer interneurons, and cerebellar efferent cells (cerebellar nucleus cells in mammals) that Purkinje cells inhibit. This modular organization is more apparent and more sharply defined in the Mormyrid than in the mammal.
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immunocytochemical identification of cell types in the Mormyrid electrosensory lobe
The Journal of Comparative Neurology, 2005Co-Authors: Curtis C Bell, J Meek, Jianji Y YangAbstract:The electrosensory lobes (ELLs) of Mormyrid and gymnotid fish are useful sites for studying plasticity and descending control of sensory processing. This study used immunocytochemistry to examine the functional circuitry of the Mormyrid ELL. We used antibodies against the following proteins and amino acids: the neurotransmitters glutamate and gamma-aminobutyric acid (GABA); the GABA-synthesizing enzyme glutamic acid decarboxylase (GAD); GABA transporter 1; the anchoring protein for GABA and glycine receptors, gephyrin; the calcium binding proteins calbindin and calretinin; the NR1 subunit of the N-methyl-D-aspartate glutamate receptor; the metabotropic glutamate receptors mGluR1alpha, mGluR2/3, and mGluR5; and the intracellular signaling molecules calcineurin, calcium calmodulin kinase IIalpha (CAMKIIalpha) and the receptor for inositol triphosphate (IP3R1alpha). Selective staining allowed for identification of new cell types including a deep granular layer cell that relays sensory information from primary afferent fibers to higher order cells of ELLS. Selective staining also allowed for estimates of relative numbers of different cell types. Dendritic staining of Purkinje-like medium ganglion cells with antibodies against metabotropic glutamate receptors and calcineurin suggests hypotheses concerning mechanisms of the previously demonstrated synaptic plasticity in these cells. Finally, several cell types including the above-mentioned granular cells, thick-smooth dendrite cells, and large multipolar cells of the intermediate layer were present in the two zones of ELL that receive input from mormyromast electroreceptors but were absent in the zone of ELL that receives input from ampullary electroreceptors, indicating markedly different processing for these two types of input. J. Comp. Neurol. 483:124-142, 2005. (c) 2005 Wiley-Liss, Inc.
Bruce A. Carlson - One of the best experts on this subject based on the ideXlab platform.
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signal diversification is associated with corollary discharge evolution in weakly electric fish
The Journal of Neuroscience, 2020Co-Authors: Matasaburo Fukutomi, Bruce A. CarlsonAbstract:Communication signal diversification is a driving force in the evolution of sensory and motor systems. However, little is known about the evolution of sensorimotor integration. Mormyrid fishes generate stereotyped electric pulses (electric organ discharge [EOD]) for communication and active sensing. The EOD has diversified extensively, especially in duration, which varies across species from 0.1 to >10 ms. In the electrosensory hindbrain, a corollary discharge that signals the timing of EOD production provides brief, precisely timed inhibition that effectively blocks responses to self-generated EODs. However, corollary discharge inhibition has only been studied in a few species, all with short-duration EODs. Here, we asked how corollary discharge inhibition has coevolved with the diversification of EOD duration. We addressed this question by comparing 7 Mormyrid species (both sexes) having varied EOD duration. For each individual fish, we measured EOD duration and then measured corollary discharge inhibition by recording evoked potentials from midbrain electrosensory nuclei. We found that delays in corollary discharge inhibition onset were strongly correlated with EOD duration as well as delay to the first peak of the EOD. In addition, we showed that electrosensory receptors respond to self-generated EODs with spikes occurring in a narrow time window immediately following the first peak of the EOD. Direct comparison of time courses between the EOD and corollary discharge inhibition revealed that the inhibition overlaps the first peak of the EOD. Our results suggest that internal delays have shifted the timing of corollary discharge inhibition to optimally block responses to self-generated signals. SIGNIFICANCE STATEMENT Corollary discharges are internal copies of motor commands that are essential for brain function. For example, corollary discharge allows an animal to distinguish self-generated from external stimuli. Despite widespread diversity in behavior and its motor control, we know little about the evolution of corollary discharges. Mormyrid fishes generate stereotyped electric pulses used for communication and active sensing. In the electrosensory pathway that processes communication signals, a corollary discharge inhibits sensory responses to self-generated signals. We found that fish with long-duration pulses have delayed corollary discharge inhibition, and that this time-shifted corollary discharge optimally blocks electrosensory responses to the fish9s own signal. Our study provides the first evidence for evolutionary change in sensorimotor integration related to diversification of communication signals.
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a history of corollary discharge contributions of Mormyrid weakly electric fish
Frontiers in Integrative Neuroscience, 2020Co-Authors: Matasaburo Fukutomi, Bruce A. CarlsonAbstract:Corollary discharge is an important brain function that allows animals to distinguish external from self-generated signals, which is critical to sensorimotor coordination. Since discovery of the concept of corollary discharge in 1950, neuroscientists have sought to elucidate underlying neural circuits and mechanisms. Here, we review a history of neurophysiological studies on corollary discharge and highlight significant contributions from studies using African Mormyrid weakly electric fish. Mormyrid fish generate brief electric pulses to communicate with other fish and to sense their surroundings. In addition, Mormyrids can passively locate weak, external electric signals. These three behaviors are mediated by different corollary discharge functions including inhibition, enhancement, and predictive "negative image" generation. Owing to several experimental advantages of Mormyrids, investigations of these mechanisms have led to important general principles that have proven applicable to a wide diversity of animal species.
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signal diversification is associated with corollary discharge evolution in weakly electric fish
The Journal of Neuroscience, 2020Co-Authors: Matasaburo Fukutomi, Bruce A. CarlsonAbstract:Communication signal diversification is a driving force in the evolution of sensory and motor systems. However, little is known about the evolution of sensorimotor integration. Mormyrid fishes generate stereotyped electric pulses (electric organ discharge [EOD]) for communication and active sensing. The EOD has diversified extensively, especially in duration, which varies across species from 0.1 to over 10 ms. In the electrosensory hindbrain, a corollary discharge that signals the timing of EOD production provides brief, precisely timed inhibition that effectively blocks responses to self-generated EODs. However, corollary discharge inhibition has only been studied in a few species, all with short duration EODs. Here, we asked how corollary discharge inhibition has coevolved with the diversification of EOD duration. We addressed this question by comparing 7 Mormyrid species (both sexes) having varied EOD duration. For each individual fish, we measured EOD duration and then measured corollary discharge inhibition by recording evoked potentials from midbrain electrosensory nuclei. We found that delays in corollary discharge inhibition onset were strongly correlated with EOD duration as well as delay to the first peak of the EOD. In addition, we showed that electrosensory receptors respond to self-generated EODs with spikes occurring in a narrow time window immediately following the first peak of the EOD. Direct comparison of time courses between the EOD and corollary discharge inhibition revealed that the inhibition overlaps the first peak of the EOD. Our results suggest that internal delays have shifted the timing of corollary discharge inhibition to optimally block responses to self-generated signals.SIGNIFICANCE STATEMENTCorollary discharges are internal copies of motor commands that are essential for brain function. For example, corollary discharge allows an animal to distinguish self-generated from external stimuli. Despite widespread diversity in behavior and its motor control, we know little about the evolution of corollary discharges. Mormyrid fishes generate stereotyped electric pulses used for communication and active sensing. In the electrosensory pathway that processes communication signals, a corollary discharge inhibits sensory responses to self-generated signals. We found that fish with long duration pulses have delayed corollary discharge inhibition, and that this time-shifted corollary discharge optimally blocks electrosensory responses to the fish's own signal. Our study provides the first evidence for evolutionary change in sensorimotor integration related to diversification of communication signals.
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signal diversification is associated with corollary discharge evolution in weakly electric fish
bioRxiv, 2020Co-Authors: Matasaburo Fukutomi, Bruce A. CarlsonAbstract:Communication signal diversification is a driving force in the evolution of sensory and motor systems. However, little is known about the evolution of sensorimotor integration. Mormyrid fishes generate stereotyped electric pulses (electric organ discharge [EOD]) for communication and active sensing. The EOD has diversified extensively, especially in duration, which varies across species from 0.1 to over 10 ms. In the electrosensory hindbrain, a corollary discharge that signals the timing of EOD production provides brief, precisely timed inhibition that effectively blocks responses to self-generated EODs. However, corollary discharge inhibition has only been studied in a few species, all with short duration EODs. Here, we asked how corollary discharge inhibition has coevolved with the diversification of EOD duration. We addressed this question by comparing 7 Mormyrid species having varied EOD duration. For each individual fish, we measured EOD duration and then measured corollary discharge inhibition by recording evoked potentials from midbrain electrosensory nuclei. We found that delays in the onset of corollary discharge inhibition were strongly correlated with EOD duration as well as delay to the first peak of the EOD. In addition, we showed that electrosensory receptors respond to self-generated EODs with spikes occurring in a narrow time window immediately following the first peak of the EOD. Direct comparison of time courses between the EOD and corollary discharge inhibition revealed that the inhibition overlaps the first peak of the EOD. Our results suggest that internal delays have shifted the timing of corollary discharge inhibition to optimally block responses to self-generated signals.
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BBE355369.indd
2020Co-Authors: S Karger, Kimberley V. Sukhum, Bruce A. Carlson, Jennifer A Stevens, Stevens / Sukhum, Carlson / Brain, Brain BehavAbstract:gests that a reduced visual system evolved with the origins of an active electrosense, and that this one particular lineage secondarily evolved an enlarged visual system. Behavioral tests revealed that this enlargement of the visual system established increased visual acuity. Thus, our findings demonstrate that different lineages of Mormyrids have evolved visual or electrosensory specializations, but that no lineages have specialized in both. This sensory divergence likely reflects fundamentally different ecologies and suggests that vision may play an especially important role in the social behavior of Mormyrids that cannot detect variation in electric signal waveform. Our findings provide an example of evolutionary change in multiple sensory systems among closely related species that lays a foundation for relating ecological adaptation to evolutionary change in multisensory perception and social behavior. Introduction Sensory systems can evolve in response to selection arising from a variety of biotic and abiotic factors. In extreme cases, differences between the environments of closely related species can lead to lineage-specific sensory Key Words Mormyrids · Electric fishes · Electrosensory system · Exterolateral nucleus · Visual acuity · Optic tectum · Optomotor response Abstract African Mormyrid fishes are by far the most diverse group of osteoglossomorph (bony tongue) fishes. Mormyrids communicate using pulses of electricity, and they process electric communication signals in the midbrain exterolateral nucleus (EL). In its ancestral form, the EL is relatively small and homogenous. In two different lineages, however, the EL expanded in size and increased in cytological complexity. This evolutionary change established the perceptual ability to distinguish variation in electric pulse waveform, which plays an important role in species recognition and mate choice. However, the sensory basis of social behavior in species with a small, homogenous EL remains unknown. Using published species descriptions, we found that species in one of these lineages have relatively large eyes. Using sectioned brains, we measured the volume of a major visual region, the optic tectum (OT), and found that this same lineage also has an enlarged OT. We also found that eye size and OT size are highly correlated across species. Phylogenetic analysis sug
Victor Z Han - One of the best experts on this subject based on the ideXlab platform.
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cell type specific plasticity at parallel fiber synapses onto purkinje cells in the posterior caudal lobe of the Mormyrid fish cerebellum
Journal of Neurophysiology, 2018Co-Authors: Yueping Zhang, Gerhard Magnus, Victor Z HanAbstract:It has been demonstrated that there are two morphological subtypes of Purkinje cells (PCs)-fan-shaped Purkinje cells (fPCs) and multipolar Purkinje cells (mPCs)-in the posterior caudal lobe of the Mormyrid fish cerebellum, but whether these cell types are also functionally distinct is unknown. Here, we have used electrophysiological and pharmacological tools in a slice preparation to demonstrate that pairing parallel fiber (PF) and climbing fiber (CF) inputs at a low frequency induces long-term depression (LTD) in fPCs but long-term potentiation (LTP) in mPCs. The induction of plasticity in both cell types required postsynaptic Ca2+ and type 1α metabotropic glutamate receptors. However, the LTD in fPCs was inducted via a calcium/calmodulin-dependent protein kinase II cascade, whereas LTP induction in mPCs required calcineurin. Moreover, the LTD in fPCs and LTP in mPCs were accompanied by changes to the corresponding paired-pulse ratios and their coefficients of variation, suggesting presynaptic modes of expression for the plasticity at PF terminals for both cell types. Hence, the synaptic plasticity at PF synapses onto PCs in the posterior caudal lobe of the Mormyrid cerebellum is cell type specific, with both pre- and postsynaptic mechanisms contributing to its induction and expression. NEW & NOTEWORTHY Much has been learnt about the cerebellar long-term depression (LTD) in the cortex. More recent work has shown that long-term potentiation (LTP) is equally important for cerebellar motor learning. Here we report for the first time that plasticity in the Mormyrid cerebellum is cell type specific, e.g., following the conventional pairing of parallel and climbing fiber inputs in an in vitro preparation leads to LTD in one Purkinje cell subtype and LTP in another.
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functional circuitry of a unique cerebellar specialization the valvula cerebelli of a Mormyrid fish
Neuroscience, 2011Co-Authors: Yun Zhang, Victor Z Han, J Meek, Z Shi, G Magnus, Jiantian QiaoAbstract:The valvula cerebelli of the Mormyrid electric fish is a useful site for the study of cerebellar function. The valvula forms a part of the electrosensory-electromotor system of this fish, a system that offers many possibilities for the study of sensory-motor integration. The valvula also has a number of histological features not present in mammals which facilitate investigation of cerebellar circuitry and its plasticity. This initial study characterizes the basic physiology and pharmacology of cells in the valvula using an in vitro slice preparation. Intrinsic properties and synaptic responses of Purkinje cells and other cell types were examined. We found that Purkinje cells fire a small narrow Na(+) spike and a large broad Ca(2+) spike, generated in the axon initial segment and dendritic-soma region, respectively. Purkinje cells respond to parallel fiber inputs with graded excitatory postsynaptic potentials (EPSPs) and to climbing fiber inputs with all-or-none EPSPs. Efferent cells, Golgi cells, and deep stellate cells all fire a single type of large narrow spike and respond only to parallel fiber inputs. Both parallel fiber and climbing fiber responses in Purkinje cells appear to be entirely mediated by AMPA-type glutamate receptors, whereas parallel fiber responses in efferent cells and stellate cells include AMPA and NMDA components. In addition, a strong synaptic inhibition was uncovered in both Purkinje cells and efferent cells in response to the focal stimulation of parallel fibers. Dual cell recordings indicate that deep stellate cells contribute at least partially to this inhibition. We conclude that despite its unique histology, the local functional circuitry of the Mormyrid valvula cerebelli is largely similar to that of the mammalian cerebellum. Thus, what is learned concerning the functioning of the Mormyrid valvula cerebelli may be expected to be informative about cerebellar function in general.
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the neuronal organization of a unique cerebellar specialization the valvula cerebelli of a Mormyrid fish
The Journal of Comparative Neurology, 2008Co-Authors: Z Shi, Yueping Zhang, J Meek, Jiantian Qiao, Victor Z HanAbstract:The distal valvula cerebelli is the most prominent part of the Mormyrid cerebellum. It is organized in ridges of ganglionic and molecular layers, oriented perpendicular to the granular layer. We have combined intracellular recording and labeling techniques to reveal the cellular morphology of the valvula ridges in slice preparations. We have also locally ejected tracer in slices and in intact animals to examine its input fibers. The palisade dendrites and fine axon arbors of Purkinje cells are oriented in the horizontal plane of the ridge. The dendrites of basal efferent cells and large central cells are confined to the molecular layer but are not planar. Basal efferent cell axons are thick and join the basal bundle leaving the cerebellum. Large central cell axons are also thick, and they traverse long distances in the transverse plane, with local collaterals in the ganglionic layer. Vertical cells and small central cells also have thick axons with local collaterals. The dendrites of Golgi cells are confined to the molecular layer, but their axon arbors are either confined to the granular layer or proliferate in both the granular and ganglionic layers. Dendrites of deep stellate cells are distributed in the molecular layer, with fine axon arbors in the ganglionic layer. Granule cell axons enter the molecular layer as parallel fibers without bifurcating. Climbing fibers run in the horizontal plane and terminate exclusively in the ganglionic layer. Our results confirm and extend previous studies and suggest a new concept of the circuitry of the Mormyrid valvula cerebelli. J. Comp. Neurol. 509:449–473, 2008. © 2008 Wiley-Liss, Inc.
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local circuitry in the anterior caudal lobe of the Mormyrid cerebellum a study of intracellular recording and labeling
The Journal of Comparative Neurology, 2008Co-Authors: Yueping Zhang, Phil F Han, Victor Z HanAbstract:The caudal lobe of the Mormyrid cerebellum includes the anterior portion, which is associated with the lateral line and eighth nerve senses, and the posterior portion, which is associated with the electrosense. This study examines the physiology and morphology of cells in the anterior portion in slice preparations. Two subtypes of Purkinje cells, efferent cells and stellate cells, are described. Multipolar Purkinje cells are located in the central region of the lobe, with large, multipolar, spiny dendrites and locally ending axons. Small Purkinje cells are located along its anterior border with the eminentia granularis anterior (EGa), with spiny dendrites in the molecular region. Axons of some small Purkinje cells end locally, whereas axons of other such cells are cut at the surface of the slices, suggesting that they project outside the lobe. Efferent cells are also distributed along the border with EGa. These cells have thin, smooth dendrites in the molecular region, and their axons are cut at the sliced surface. Stellate cells have thin, smooth dendrites and locally terminating axons. Physiologically, all types of cells respond to parallel fiber activation, but only multipolar Purkinje cells showed characteristic all-or-none climbing fiber responses. Although the majority of Purkinje cells fire a single type of spikes at resting level, a subset of small Purkinje cells fire small, narrow and large, broad spikes. Thus, the anterior caudal lobe of the Mormyrid cerebellum is different from the mammalian cerebellum in having different subtypes of Purkinje cells and local termination of many Purkinje cell axons.
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synaptic plasticity and calcium signaling in purkinje cells of the central cerebellar lobes of Mormyrid fish
The Journal of Neuroscience, 2007Co-Authors: Victor Z Han, Curtis C Bell, Yueping Zhang, Christian HanselAbstract:Climbing fiber (CF)-evoked calcium transients play a key role in plasticity at parallel fiber (PF) to Purkinje cell synapses in the mammalian cerebellum. Whereas PF activation alone causes long-term potentiation (LTP), coactivation of the heterosynaptic CF input, which evokes large dendritic calcium transients, induces long-term depression (LTD). This unique type of heterosynaptic interaction is a hallmark feature of synaptic plasticity in mammalian Purkinje cells. Purkinje cells in the cerebellum of Mormyrid electric fish are characterized by a different architecture of their dendritic trees and by a more pronounced separation of CF and PF synaptic contact sites. We therefore examined the conditions for bidirectional plasticity at PF synapses onto Purkinje cells in the Mormyrid cerebellum in vitro. PF stimulation at elevated frequencies induces LTP, whereas LTD results from PF stimulation at enhanced intensities and depends on dendritic calcium influx and metabotropic glutamate receptor type 1 activation. LTD can also be observed after pairing of low intensity PF stimulation with CF stimulation. Using a combination of whole-cell patch-clamp recordings and fluorometric calcium imaging, we characterized calcium transients in Purkinje cell dendrites. CF activation elicits calcium transients not only within the CF input territory (smooth proximal dendrites) but also within the PF input territory (spiny palisade dendrites). Paired PF and CF activation elicits larger calcium transients than stimulation of either input alone. A major source for dendritic calcium signaling is provided by P/Q-type calcium channels. Our data show that despite the spatial separation between the two inputs CF activity facilitates LTD induction at PF synapses.