Spike timing-dependent plasticity alters electrosensory neuron synaptic strength in vitro but does not consistently predict changes in sensory tuning in vivo.

How do sensory systems optimize detection of behaviorally relevant stimuli when the sensory environment is constantly changing? We addressed the role of spike timing-dependent plasticity (STDP) in driving changes in synaptic strength in a sensory pathway and whether those changes in synaptic strength could alter sensory tuning. It is challenging to precisely control temporal patterns of synaptic activity in vivo and replicate those patterns in vitro in behaviorally relevant ways. This makes it difficult to make connections between STDP-induced changes in synaptic physiology and plasticity in sensory systems. Using the mormyrid species Brevimyrus niger and Brienomyrus brachyistius, which produce electric organ discharges for electrolocation and communication, we can precisely control the timing of synaptic input in vivo and replicate these same temporal patterns of synaptic input in vitro. In central electrosensory neurons in the electric communication pathway, using whole cell intracellular recordings in vitro, we paired presynaptic input with postsynaptic spiking at different delays. Using whole cell intracellular recordings in awake, behaving fish, we paired sensory stimulation with postsynaptic spiking using the same delays. We found that Hebbian STDP predictably alters sensory tuning in vitro and is mediated by NMDA receptors. However, the change in synaptic responses induced by sensory stimulation in vivo did not adhere to the direction predicted by the STDP observed in vitro. Further analysis suggests that this difference is influenced by polysynaptic activity, including inhibitory interneurons. Our findings suggest that STDP rules operating at identified synapses may not drive predictable changes in sensory responses at the circuit level.NEW & NOTEWORTHY We replicated behaviorally relevant temporal patterns of synaptic activity in vitro and used the same patterns during sensory stimulation in vivo. There was a Hebbian spike timing-dependent plasticity (STDP) pattern in vitro, but sensory responses in vivo did not shift according to STDP predictions. Analysis suggests that this disparity is influenced by differences in polysynaptic activity, including inhibitory interneurons. These results suggest that STDP rules at synapses in vitro do not necessarily apply to circuits in vivo.

Evolutionary divergence of developmental plasticity and learning of mating tactics in Trinidadian guppies.

Behavioural plasticity is a major driver in the early stages of adaptation, but its effects in mediating evolution remain elusive because behavioural plasticity itself can evolve. In this study, we investigated how male Trinidadian guppies (Poecilia reticulata) adapted to different predation regimes diverged in behavioural plasticity of their mating tactic. We reared F2 juveniles of high- or low-predation population origins with different combinations of social and predator cues and assayed their mating behaviour upon sexual maturity. High-predation males learned their mating tactic from conspecific adults as juveniles, while low-predation males did not. High-predation males increased courtship when exposed to chemical predator cues during development; low-predation males decreased courtship in response to immediate chemical predator cues, but only when they were not exposed to such cues during development. Behavioural changes induced by predator cues were associated with developmental plasticity in brain morphology, but changes acquired through social learning were not. We thus show that guppy populations diverged in their response to social and ecological cues during development, and correlational evidence suggests that different cues can shape the same behaviour via different neural mechanisms. Our study demonstrates that behavioural plasticity, both environmentally induced and socially learnt, evolves rapidly and shapes adaptation when organisms colonize ecologically divergent habitats.

La plasticidad conductual es un factor importante en las primeras fases de adaptación, pero se conocen poco sus efectos sobre la evolución porque la plasticidad conductual en sí puede evolucionar. En este estudio, investigamos cómo los machos del guppy de Trinidad (Poecilia reticulata) adaptados a regímenes de depredación diferentes, han divergido en la plasticidad de su táctica de apareamiento. Criamos juveniles provenientes de poblaciones de alta y baja depredación hasta segunda generación (F2) bajo diferentes combinaciones de señales sociales y de depredación, y evaluamos su comportamiento de apareamiento al llegar a la madurez sexual. Los machos de alta depredación aprendieron su táctica de apareamiento de sus conespecíficos adultos, mientras que los machos de baja depredación no. Los machos de alta depredación aumentaron su cortejo al ser expuestos a señales de depredadores durante su desarrollo; mientras que los machos de baja depredación redujeron su cortejo en respuesta a señales inmediatas de depredadores, pero tan solo cuando no fueron expuestos a tales señales durante el desarrollo. Los cambios conductuales observados inducidos por las señales de depredación están asociados con una plasticidad en el desarrollo de la morfología cerebral, pero los cambios adquiridos por aprendizaje social no. En conclusión, demostramos que las poblaciones de guppy han divergido en su respuesta a señales sociales y ecológicas durante su desarrollo, y mostramos evidencia correlativa que sugiere que diferentes tipos de señales pueden influenciar el mismo comportamiento via mecanismos neuronales diferentes. Nuestro estudio muestra que la plasticidad conductual, tanto inducida por el medio ambiente combo aprendida socialmente, evoluciona rápidamente e influencia la adaptación durante la colonización de hábitats ecológicamente divergentes.

Signal Diversification Is Associated with Corollary Discharge Evolution in Weakly Electric Fish.

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 fish's own signal. Our study provides the first evidence for evolutionary change in sensorimotor integration related to diversification of communication signals.

Intraspecific Energetic Trade-Offs and Costs of Encephalization Vary from Interspecific Relationships in Three Species of Mormyrid Electric Fishes.

The evolution of increased encephalization comes with an energetic cost. Across species, this cost may be paid for by an increase in metabolic rate or by energetic trade-offs between the brain and other energy-expensive tissues. However, it remains unclear whether these solutions to deal with the energetic requirements of an enlarged brain are related to direct physiological constraints or other evolved co-adaptations. We studied the highly encephalized mormyrid fishes, which have extensive species diversity in relative brain size. We previously found a correlation between resting metabolic rate and relative brain size across species; however, it is unknown how this interspecific relationship evolved. To address this issue, we measured intraspecific variation in relative brain size, the sizes of other organs, metabolic rate, and hypoxia tolerance to determine if intraspecific relationships between brain size and organismal energetics are similar to interspecific relationships. We found that 3 species of mormyrids with varying degrees of encephalization had no intraspecific relationships between relative brain size and relative metabolic rate or relative sizes of other organs, and only 1 species had a relationship between relative brain size and hypoxia tolerance. These species-specific differences suggest that the interspecific relationship between metabolic rate and relative brain size is not the result of direct physiological constraints or strong stabilizing selection, but is instead due to other species level co-adaptations. We conclude that variation within species must be considered when determining the energetic costs and trade-offs underlying the evolution of extreme encephalization.

Sensory Specializations of Mormyrid Fish Are Associated with Species Differences in Electric Signal Localization Behavior.

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.

Behavioral and Single-Neuron Sensitivity to Millisecond Variations in Temporally Patterned Communication Signals.

UNLABELLED: 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'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.

The costs of a big brain: extreme encephalization results in higher energetic demand and reduced hypoxia tolerance in weakly electric African fishes.

A large brain can offer several cognitive advantages. However, brain tissue has an especially high metabolic rate. Thus, evolving an enlarged brain requires either a decrease in other energetic requirements, or an increase in overall energy consumption. Previous studies have found conflicting evidence for these hypotheses, leaving the metabolic costs and constraints in the evolution of increased encephalization unclear. Mormyrid electric fishes have extreme encephalization comparable to that of primates. Here, we show that brain size varies widely among mormyrid species, and that there is little evidence for a trade-off with organ size, but instead a correlation between brain size and resting oxygen consumption rate. Additionally, we show that increased brain size correlates with decreased hypoxia tolerance. Our data thus provide a non-mammalian example of extreme encephalization that is accommodated by an increase in overall energy consumption. Previous studies have found energetic trade-offs with variation in brain size in taxa that have not experienced extreme encephalization comparable with that of primates and mormyrids. Therefore, we suggest that energetic trade-offs can only explain the evolution of moderate increases in brain size, and that the energetic requirements of extreme encephalization may necessitate increased overall energy investment.

Differences in electrosensory anatomy and social behavior in an area of sympatry between two species of mormyrid electric fishes.

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.

Short-term depression, temporal summation, and onset inhibition shape interval tuning in midbrain neurons.

A variety of synaptic mechanisms can contribute to single-neuron selectivity for temporal intervals in sensory stimuli. However, it remains unknown how these mechanisms interact to establish single-neuron sensitivity to temporal patterns of sensory stimulation in vivo. Here we address this question in a circuit that allows us to control the precise temporal patterns of synaptic input to interval-tuned neurons in behaviorally relevant ways. We obtained in vivo intracellular recordings under multiple levels of current clamp from midbrain neurons in the mormyrid weakly electric fish Brienomyrus brachyistius during stimulation with electrosensory pulse trains. To reveal the excitatory and inhibitory inputs onto interval-tuned neurons, we then estimated the synaptic conductances underlying responses. We found short-term depression in excitatory and inhibitory pathways onto all interval-tuned neurons. Short-interval selectivity was associated with excitation that depressed less than inhibition at short intervals, as well as temporally summating excitation. Long-interval selectivity was associated with long-lasting onset inhibition. We investigated tuning after separately nullifying the contributions of temporal summation and depression, and found the greatest diversity of interval selectivity among neurons when both mechanisms were at play. Furthermore, eliminating the effects of depression decreased sensitivity to directional changes in interval. These findings demonstrate that variation in depression and summation of excitation and inhibition helps to establish tuning to behaviorally relevant intervals in communication signals, and that depression contributes to neural coding of interval sequences. This work reveals for the first time how the interplay between short-term plasticity and temporal summation mediates the decoding of temporal sequences in awake, behaving animals.

Diversity of intraspecific patterns of brain region size covariation in fish.

Traits often do not evolve in isolation or vary independently of other traits. Instead, they can be affected by covariation, both within and across species. However, the importance of within species trait covariation and, critically, the degree to which it varies between species has yet to be thoroughly studied. Brain morphology is a trait of great ecological and behavioral importance, with regions that are hypothesized to vary in size based on behavioral and cognitive demands. Sizes of brain regions have also been shown to covary with each other across various taxa. Here we test the degree to which covariation in brain region sizes within species has been conserved across ten teleost fish species. These ten species span five orders, allowing us to examine how phylogenetic proximity influences similarities in intraspecific trait covariation. Our results showed a trend that similar patterns of brain region size covariation occur in more closely related species. Interestingly, there were certain brain region pairs that showed similar levels of covariation across all species regardless of phylogenetic distance, such as the telencephalon and optic tectum, while others, such as the olfactory bulb and the hypothalamus, varied more independently. Ultimately, the patterns of brain region covariation shown here suggest that evolutionary mechanisms or constraints can act on specific brain regions independently, and that these constraints can change over evolutionary time.

Evolutionary divergence of plasticity in brain morphology between ecologically divergent habitats of Trinidadian guppies.

Phenotypic plasticity is critical for organismal performance and can evolve in response to natural selection. Brain morphology is often developmentally plastic, affecting animal performance in a variety of contexts. However, the degree to which the plasticity of brain morphology evolves has rarely been explored. Here, we use Trinidadian guppies (Poecilia reticulata), which are known for their repeated adaptation to high-predation (HP) and low-predation (LP) environments, to examine the evolution and plasticity of brain morphology. We exposed second-generation offspring of individuals from HP and LP sites to 2 different treatments: predation cues and conspecific social environment. Results show that LP guppies had greater plasticity in brain morphology compared to their ancestral HP population, suggesting that plasticity can evolve in response to environmentally divergent habitats. We also show sexual dimorphism in the plasticity of brain morphology, highlighting the importance of considering sex-specific variation in adaptive diversification. Overall, these results may suggest the evolution of brain morphology plasticity as an important mechanism that allows for ecological diversification and adaptation to divergent habitats.

How do short-term changes at synapses fine-tune information processing?

Synaptic transmission is highly dependent on recent activity and can lead to depression or facilitation of synaptic strength. This phenomenon is called "short-term synaptic plasticity" and is shown at all synapses. While much work has been done to understand the mechanisms of short-term changes in the state of synapses, short-term plasticity is often thought of as a mechanistic consequence of the design of a synapse. This review will attempt to go beyond this view and discuss how, on one hand, complex neuronal activity affects the short-term state of synapses, but also how these dynamic changes in synaptic strength affect information processing in return.

Extensive excitatory network interactions shape temporal processing of communication signals in a model sensory system.

Many sensory brain regions are characterized by extensive local network interactions. However, we know relatively little about the contribution of this microcircuitry to sensory coding. Detailed analyses of neuronal microcircuitry are usually performed in vitro, whereas sensory processing is typically studied by recording from individual neurons in vivo. The electrosensory pathway of mormyrid fish provides a unique opportunity to link in vitro studies of synaptic physiology with in vivo studies of sensory processing. These fish communicate by actively varying the intervals between pulses of electricity. Within the midbrain posterior exterolateral nucleus (ELp), the temporal filtering of afferent spike trains establishes interval tuning by single neurons. We characterized pairwise neuronal connectivity among ELp neurons with dual whole cell recording in an in vitro whole brain preparation. We found a densely connected network in which single neurons influenced the responses of other neurons throughout the network. Similarly tuned neurons were more likely to share an excitatory synaptic connection than differently tuned neurons, and synaptic connections between similarly tuned neurons were stronger than connections between differently tuned neurons. We propose a general model for excitatory network interactions in which strong excitatory connections both reinforce and adjust tuning and weak excitatory connections make smaller modifications to tuning. The diversity of interval tuning observed among this population of neurons can be explained, in part, by each individual neuron receiving a different complement of local excitatory inputs.

Detection of submillisecond spike timing differences based on delay-line anticoincidence detection.

Detection of submillisecond interaural timing differences is the basis for sound localization in reptiles, birds, and mammals. Although comparative studies reveal that different neural circuits underlie this ability, they also highlight common solutions to an inherent challenge: processing information on timescales shorter than an action potential. Discrimination of small timing differences is also important for species recognition during communication among mormyrid electric fishes. These fishes generate a species-specific electric organ discharge (EOD) that is encoded into submillisecond-to-millisecond timing differences between receptors. Small, adendritic neurons (small cells) in the midbrain are thought to analyze EOD waveform by comparing these differences in spike timing, but direct recordings from small cells have been technically challenging. In the present study we use a fluorescent labeling technique to obtain visually guided extracellular recordings from individual small cell axons. We demonstrate that small cells receive 1-2 excitatory inputs from 1 or more receptive fields with latencies that vary by over 10 ms. This wide range of excitatory latencies is likely due to axonal delay lines, as suggested by a previous anatomic study. We also show that inhibition of small cells from a calyx synapse shapes stimulus responses in two ways: through tonic inhibition that reduces spontaneous activity and through precisely timed, stimulus-driven, feed-forward inhibition. Our results reveal a novel delay-line anticoincidence detection mechanism for processing submillisecond timing differences, in which excitatory delay lines and precisely timed inhibition convert a temporal code into a population code.

From sequence to spike to spark: evo-devo-neuroethology of electric communication in mormyrid fishes.

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.

Multiplexed temporal coding of electric communication signals in mormyrid fishes.

The 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.

Independent evolution of visual and electrosensory specializations in different lineages of mormyrid electric fishes.

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.

Hormonal coordination of motor output and internal prediction of sensory consequences in an electric fish.

Steroid hormones remodel neural networks to induce seasonal or developmental changes in behavior. Hormonal changes in behavior likely require coordinated changes in sensorimotor integration. Here, we investigate hormonal effects on a predictive motor signal, termed corollary discharge, that modulates sensory processing in weakly electric mormyrid fish. In the electrosensory pathway mediating communication behavior, inhibition activated by a corollary discharge blocks sensory responses to self-generated electric pulses, allowing the downstream circuit to selectively analyze communication signals from nearby fish. These pulses are elongated by increasing testosterone levels in males during the breeding season. We induced electric-pulse elongation using testosterone treatment and found that the timing of electroreceptor responses to self-generated pulses was delayed as electric-pulse duration increased. Simultaneous recordings from an electrosensory nucleus and electromotor neurons revealed that the timing of corollary discharge inhibition was delayed and elongated by testosterone. Furthermore, this shift in the timing of corollary discharge inhibition was precisely matched to the shift in timing of receptor responses to self-generated pulses. We then asked whether the shift in inhibition timing was caused by direct action of testosterone on the corollary discharge circuit or by plasticity acting on the circuit in response to altered sensory feedback. We surgically silenced the electric organ of fish and found similar hormonal modulation of corollary discharge timing between intact and silent fish, suggesting that sensory feedback was not required for this shift. Our findings demonstrate that testosterone directly regulates motor output and internal prediction of the resulting sensory consequences in a coordinated manner.

Integrating neuroplasticity and evolution.

Neuroplasticity and evolutionary biology have been prominent fields of study for well over a century. However, they have advanced largely independently, without consideration of the benefits of integration. We propose a new framework by which researchers can begin to examine the evolutionary causes and consequences of neuroplasticity. Neuroplasticity can be defined as changes to the structure, function or connections of the nervous system in response to individual experience. Evolution can alter levels of neuroplasticity if there is variation in neuroplasticity traits within and between populations. Neuroplasticity may be favored or disfavored by natural selection depending on the variability of the environment and the costs of neuroplasticity. Additionally, neuroplasticity may affect rates of genetic evolution in many ways: for example, decreasing rates of evolution by buffering against selection or increasing them via the Baldwin effect, by increasing genetic variation or by incorporating evolved peripheral changes to the nervous system. These mechanisms can be tested using comparative and experimental approaches and by examining patterns and consequences of variation in neuroplasticity among species, populations and individuals.