@article {572, title = {Sensory Specializations of Mormyrid Fish Are Associated with Species Differences in Electric Signal Localization Behavior}, journal = {Brain, Behavior and Evolution}, year = {2019}, month = {Jan-03-2019}, pages = {1 - 17}, abstract = {

The ability to localize communication signals plays a fundamental role in social interactions. For signal localization to take place, the sensory system of the receiver must extract information about distance and direction to the sender from physical characteristics of the signal. In many sensory systems, information from multiple peripheral receptors must be integrated by central sensory pathways to determine the sender location. Here, we asked whether evolutionary divergence in the electrosensory and visual systems of mormyrid fish is associated with signal localization behavior. In mormyrids, differences in the distribution of electroreceptors on the surface of the skin are associated with differences in the midbrain exterolateral nucleus (EL). Species with electroreceptors clustered in three rosettes on both sides of the head have a small and undifferentiated EL. In contrast, EL is enlarged and subdivided into anterior (ELa) and posterior (ELp) regions in species that have electroreceptors broadly \­distributed throughout the body. Interestingly, species with EL and clustered electroreceptors also have larger visual systems and higher visual acuity than species with ELa/ELp and broadly distributed electroreceptors. Species with broadly distributed electroreceptors and ELa/ELp approached a simulated conspecific by following the curved electric field lines generated by the electrosensory stimulus. In contrast, a species with small EL and clustered electroreceptors, but an enlarged visual system, followed shorter and straighter paths to the stimulus source. In the central electrosensory system, evoked field potentials in response to stimuli delivered from the left versus the right differed more in EL than in ELa/ELp. Our results suggest that signal localization behavior is associated with differences in sensory specializations. We propose that the distribution of electroreceptors on the body affects the ability of individuals to align parallel to electric field lines and maintain such alignment while approaching the signal source. The spatial resolution of sensory information relayed from the periphery to the midbrain in species with clustered electroreceptors may allow for gross, but not fine, processing of sender location. Furthermore, visual information may play an important role in localizing signaling individuals in species with small EL and clustered electroreceptors. In line with previous studies, we suggest that the physiological and behavioral differences associated with signal localization reflect adaptations to different habitats and social environments.

}, issn = {0006-8977}, doi = {10.1159/000496493}, url = {https://www.karger.com/Article/FullText/496493https://www.karger.com/Article/Pdf/496493https://www.karger.com/Article/Pdf/496493}, author = {V{\'e}lez, Alejandro and Ryoo, Da~Yeon and Bruce A. Carlson} } @article {537, title = {Behavioral and Single-Neuron Sensitivity to Millisecond Variations in Temporally Patterned Communication Signals}, journal = {Journal of Neuroscience}, volume = {36}, year = {2016}, month = {Feb-16-20162220}, pages = {8985 - 9000}, abstract = {

In many sensory pathways, central neurons serve as temporal filters for timing patterns in communication signals. However, how a population of neurons with diverse temporal filtering properties codes for natural variation in communication signals is unknown. Here we addressed this question in the weakly electric fish Brienomyrus brachyistius, which varies the time intervals between successive electric organ discharges to communicate. These fish produce an individually stereotyped signal called a scallop, which consists of a distinctive temporal pattern of \∼8\–12 electric pulses. We manipulated the temporal structure of natural scallops during behavioral playback and in vivo electrophysiology experiments to probe the temporal sensitivity of scallop encoding and recognition. We found that presenting time-reversed, randomized, or jittered scallops increased behavioral response thresholds, demonstrating that fish\&$\#$39;s electric signaling behavior was sensitive to the precise temporal structure of scallops. Next, using in vivo intracellular recordings and discriminant function analysis, we found that the responses of interval-selective midbrain neurons were also sensitive to the precise temporal structure of scallops. Subthreshold changes in membrane potential recorded from single neurons discriminated natural scallops from time-reversed, randomized, and jittered sequences. Pooling the responses of multiple neurons improved the discriminability of natural sequences from temporally manipulated sequences. Finally, we found that single-neuron responses were sensitive to interindividual variation in scallop sequences, raising the question of whether fish may analyze scallop structure to gain information about the sender. Collectively, these results demonstrate that a population of interval-selective neurons can encode behaviorally relevant temporal patterns with millisecond precision.

SIGNIFICANCE STATEMENT The timing patterns of action potentials, or spikes, play important roles in representing information in the nervous system. However, how these temporal patterns are recognized by downstream neurons is not well understood. Here we use the electrosensory system of mormyrid weakly electric fish to investigate how a population of neurons with diverse temporal filtering properties encodes behaviorally relevant input timing patterns, and how this relates to behavioral sensitivity. We show that fish are behaviorally sensitive to millisecond variations in natural, temporally patterned communication signals, and that the responses of individual midbrain neurons are also sensitive to variation in these patterns. In fact, the output of single neurons contains enough information to discriminate stereotyped communication signals produced by different individuals.

}, issn = {0270-6474}, doi = {10.1523/JNEUROSCI.0648-16.2016}, url = {http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.0648-16.2016}, author = {Baker, C. A. and Ma, L. and Casareale, C. R. and Bruce A. Carlson} } @article {534, title = {Detection of transient synchrony across oscillating receptors by the central electrosensory system of mormyrid fish}, journal = {eLife}, volume = {5}, year = {2016}, month = {Sep-06-2017}, abstract = {

Recently, we reported evidence for a novel mechanism of peripheral sensory coding based on oscillatory synchrony. Spontaneously oscillating electroreceptors in weakly electric fish (Mormyridae) respond to electrosensory stimuli with a phase reset that results in transient synchrony across the receptor population (Baker et al., 2015). Here, we asked whether the central electrosensory system actually detects the occurrence of synchronous oscillations among receptors. We found that electrosensory stimulation elicited evoked potentials in the midbrain exterolateral nucleus at a short latency following receptor synchronization. Frequency tuning in the midbrain resembled peripheral frequency tuning, which matches the intrinsic oscillation frequencies of the receptors. These frequencies are lower than those in individual conspecific signals, and instead match those found in collective signals produced by groups of conspecifics. Our results provide further support for a novel mechanism for sensory coding based on the detection of oscillatory synchrony among peripheral receptors.

}, doi = {10.7554/eLife.16851}, url = {http://elifesciences.org/lookup/doi/10.7554/eLife.16851}, author = {V{\'e}lez, Alejandro and Bruce A. Carlson} } @article {485, title = {Differences in electrosensory anatomy and social behavior in an area of sympatry between two species of mormyrid electric fishes}, journal = {Journal of Experimental Biology}, volume = {219}, year = {2016}, month = {Apr-11-2016}, pages = {31 - 43}, abstract = {

Sensory systems play a key role in social behavior by mediating the detection and analysis of communication signals. In mormyrid fishes, electric signals are processed within a dedicated sensory pathway, providing a unique opportunity to relate sensory biology to social behavior. Evolutionary changes within this pathway led to new perceptual abilities that have been linked to increased rates of signal evolution and species diversification in a lineage called \‘clade A\’. Previous field observations suggest that clade-A species tend to be solitary and territorial, whereas non-clade-A species tend to be clustered in high densities suggestive of schooling or shoaling. To explore behavioral differences between species in these lineages in greater detail, I studied population densities, social interactions, and electric signaling in two mormyrid species, Gnathonemus victoriae (clade A) and Petrocephalus degeni (non-clade A), from Lwamunda Swamp, Uganda. Petrocephalus degeni was found at higher population densities, but intraspecific diversity in electric signal waveform was greater in G. victoriae. In the laboratory, G. victoriae exhibited strong shelter-seeking behavior and competition for shelter, whereas P. degeni were more likely to abandon shelter in the presence of conspecifics as well as electric mimics of signaling conspecifics. In other words, P. degeni exhibited social affiliation whereas G. victoriae exhibited social competition. Further, P. degeni showed correlated electric signaling behavior whereas G. victoriae showed anti-correlated signaling behavior. These findings extend previous reports of social spacing, territoriality, and habitat preference among mormyrid species, suggesting that evolutionary divergence in electrosensory processing relates to differences in social behavior.

}, issn = {0022-0949}, doi = {10.1242/jeb.127720}, url = {http://jeb.biologists.org/cgi/doi/10.1242/jeb.127720}, author = {Bruce A. Carlson} } @article {477, title = {Independent Evolution of Visual and Electrosensory Specializations in Different Lineages of Mormyrid Electric Fishes}, journal = {Brain, Behavior and Evolution}, volume = {82}, year = {2013}, month = {Jan-01-2013}, pages = {185 - 198}, 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 suggests 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.

}, issn = {0006-8977}, doi = {10.1159/000355369}, url = {http://www.karger.com?doi=10.1159/000355369}, author = {Stevens, Jennifer A. and Sukhum, Kimberley V. and Bruce A. Carlson} } @article {138, title = {Electric organ discharge patterns during group hunting by a mormyrid fish}, journal = {Proceedings of the Royal Society B}, volume = {272}, year = {2005}, pages = {1305-1314}, author = {Matthew E. Arnegard and Bruce A. Carlson} } @article {Carlson:2011if, title = {Neural innovations and the diversification of African weakly electric fishes.}, journal = {Communicative {\&} integrative biology}, volume = {4}, number = {6}, year = {2011}, pages = {720{\textendash}725}, abstract = {

In African mormyrid fishes, evolutionary change in a sensory region of the brain established an ability to detect subtle variation in electric communication signals. In one lineage, this newfound perceptual ability triggered a dramatic increase in the rates of signal evolution and species diversification. This particular neural innovation is just one in a series of nested evolutionary novelties that characterize the sensory and motor systems of mormyrids, the most speciose group of extant osteoglossomorph fishes. Here we discuss the behavioral significance of these neural innovations, relate them to differences in extant species diversity, and outline possible scenarios by which some of these traits may have fueled diversification. We propose that sensory and motor capabilities limit the extent to which signals evolve and, by extension, the role of communication behavior in the process of speciation. By expanding these capabilities, neural innovations increase the potential for signal evolution and species diversification.

}, doi = {10.4161/cib.4.6.17483}, url = {http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?}, author = {Bruce A. Carlson and Matthew E. Arnegard} } @article {Carlson:2011gd, title = {Brain Evolution Triggers Increased Diversification of Electric Fishes}, journal = {Science}, volume = {332}, number = {6029}, year = {2011}, pages = {583{\textendash}586}, abstract = {

Communication can contribute to the evolution of biodiversity by promoting speciation and reinforcing reproductive isolation between existing species. The evolution of species-specific signals depends on the ability of individuals to detect signal variation, which in turn relies on the capability of the brain to process signal information. Here, we show that evolutionary change in a region of the brain devoted to the analysis of communication signals in mormyrid electric fishes improved detection of subtle signal variation and resulted in enhanced rates of signal evolution and species diversification. These results show that neural innovations can drive the diversification of signals and promote speciation.

}, doi = {10.1126/science.1201524}, url = {http://www.sciencemag.org/cgi/doi/10.1126/science.1201524}, author = {Bruce A. Carlson and Hasan, S M and Hollmann, M and Miller, D B and Luke J. Harmon and Matthew E. Arnegard} } @article {854, title = {From Sequence to Spike to Spark: Evo-devo-neuroethology of Electric Communication in Mormyrid Fishes}, journal = {Journal of Neurogenetics}, volume = {27}, year = {2013}, month = {09/2013}, pages = {106 - 129}, abstract = {

Mormyrid fishes communicate using pulses of electricity, conveying information about their identity, behavioral state, and location. They have long been used as neuroethological model systems because they are uniquely suited to identifying cellular mechanisms for behavior. They are also remarkably diverse, and they have recently emerged as a model system for studying how communication systems may influence the process of speciation. These two lines of inquiry have now converged, generating insights into the neural basis of evolutionary change in behavior, as well as the influence of sensory and motor systems on behavioral diversification and speciation. Here, we review the mechanisms of electric signal generation, reception, and analysis and relate these to our current understanding of the evolution and development of electromotor and electrosensory systems. We highlight the enormous potential of mormyrids for studying evolutionary developmental mechanisms of behavioral diversification, and make the case for developing genomic and transcriptomic resources. A complete mormyrid genome sequence would enable studies that extend our understanding of mormyrid behavior to the molecular level by linking morphological and physiological mechanisms to their genetic basis. Applied in a comparative framework, genomic resources would facilitate analysis of evolutionary processes underlying mormyrid diversification, reveal the genetic basis of species differences in behavior, and illuminate the origins of a novel vertebrate sensory and motor system. Genomic approaches to studying the evo-devo-neuroethology of mormyrid communication represent a deeply integrative approach to understanding the evolution, function, development, and mechanisms of behavior.

}, issn = {1563-5260}, doi = {10.3109/01677063.2013.799670}, url = {http://informahealthcare.com/doi/abs/10.3109/01677063.2013.799670}, author = {Bruce A. Carlson and Jason R. Gallant} }