Ontogeny of the electric organ discharge and of the papillae of the electrocytes in the weakly electric fish Campylomormyrus rhynchophorus (Teleostei: Mormyridae).

The electric organ of the mormyrid weakly electric fish, Campylomormyrus rhynchophorus (Boulenger, 1898), undergoes changes in both the electric organ discharge (EOD) and the light and electron microscopic morphology as the fish mature from the juvenile to the adult form. Of particular interest was the appearance of papillae, surface specializations of the uninnervated anterior face of the electrocyte, which have been hypothesized to increase the duration of the EOD. In a 24.5 mm long juvenile the adult electric organ (EO) was not yet functional, and the electrocytes lacked papillae. A 40 mm long juvenile, which produced a short biphasic EOD of 1.3 ms duration, shows small papillae (average area 136 µm2 ). In contrast, the EOD of a 79 mm long juvenile was triphasic. The large increase in duration of the EOD to 23.2 ms was accompanied by a small change in size of the papillae (average area 159 µm2 ). Similarly, a 150 mm long adult produced a triphasic EOD of comparable duration to the younger stage (24.7 ms) but featured a prominent increase in size of the papillae (average area 402 µm2 ). Thus, there was no linear correlation between EOD duration and papillary size. The most prominent ultrastructural change was at the level of the myofilaments, which regularly extended into the papillae, only in the oldest specimen-probably serving a supporting function. Physiological mechanisms, like gene expression levels, as demonstrated in some Campylomormyrus species, might be more important concerning the duration of the EOD.

Intragenus F1-hybrids of African weakly electric fish (Mormyridae: Campylomormyrus tamandua ♂ × C. compressirostris ♀) are fertile.

Hybridization is widespread in fish and constitutes an important mechanism in fish speciation. There is, however, little knowledge about hybridization in mormyrids. F1-interspecies hybrids between Campylomormyrus tamandua ♂ × C. compressirostris ♀ were investigated concerning: (1) fertility; (2) survival of F2-fish and (3) new gene combinations in the F2-generation concerning the structure of the electric organ and features of the electric organ discharge. These F1-hybrids achieved sexual maturity at about 12-13.5 cm total length. A breeding group comprising six males and 13 females spawned 28 times naturally proving these F1-fish to be fertile. On average 228 eggs were spawned, the average fertilization rate was 47.8%. Eggs started to hatch 70-72 h after fertilization, average hatching rate was 95.6%. Average mortality rate during embryonic development amounted to 2.3%. Average malformation rate during the free embryonic stage was 27.7%. Exogenous feeding started on day 11. In total, we raised 353 normally developed larvae all of which died consecutively, the oldest specimen reaching an age of 5 months. During survival, the activities of the larval and adult electric organs were recorded and the structure of the adult electric organ was investigated histologically.

Calbindin-D28k expression in spinal electromotoneurons of the weakly electric fish Apteronotus leptorhynchus during adult development and regeneration.

Additive neurogenesis, the net increase in neuronal numbers by addition of new nerve cells to existing tissue, forms the basis for indeterminate spinal cord growth in brown ghost knifefish (Apteronotus leptorhynchus). Among the cells generated through the activity of adult neural stem cells are electromotoneurons, whose axons constitute the electric organ of this weakly electric fish. Electromotoneuron development is organized along a caudo-rostral gradient, with the youngest and smallest of these cells located near the caudal end of the spinal cord. Electromotoneurons start expressing calbindin-D28k when their somata have reached diameters of approximately 10 µm, and they continue expression after they have grown to a final size of about 50 µm. Calbindin-D28k expression is significantly increased in young neurons generated in response to injury. Immunohistochemical staining against caspase-3 revealed that electromotoneurons in both intact and regenerating spinal cord are significantly less likely to undergo apoptosis than the average spinal cord cell. We hypothesize that expression of calbindin-D28k protects electromotoneurons from cell death; and that the evolutionary development of such a neuroprotective mechanism has been driven by the indispensability of electromotoneurons in the fish's electric behavior, and by the high size-dependent costs associated with their production or removal upon cell death.

Molecular tuning of electroreception in sharks and skates.

Ancient cartilaginous vertebrates, such as sharks, skates and rays, possess specialized electrosensory organs that detect weak electric fields and relay this information to the central nervous system1-4. Sharks exploit this sensory modality for predation, whereas skates may also use it to detect signals from conspecifics 5 . Here we analyse shark and skate electrosensory cells to determine whether discrete physiological properties could contribute to behaviourally relevant sensory tuning. We show that sharks and skates use a similar low threshold voltage-gated calcium channel to initiate cellular activity but use distinct potassium channels to modulate this activity. Electrosensory cells from sharks express specially adapted voltage-gated potassium channels that support large, repetitive membrane voltage spikes capable of driving near-maximal vesicular release from elaborate ribbon synapses. By contrast, skates use a calcium-activated potassium channel to produce small, tunable membrane voltage oscillations that elicit stimulus-dependent vesicular release. We propose that these sensory adaptations support amplified indiscriminate signal detection in sharks compared with selective frequency detection in skates, potentially reflecting the electroreceptive requirements of these elasmobranch species. Our findings demonstrate how sensory systems adapt to suit the lifestyle or environmental niche of an animal through discrete molecular and biophysical modifications.

Draft de novo transcriptome assembly and proteome characterization of the electric lobe of Tetronarce californica: a molecular tool for the study of cholinergic neurotransmission in the electric organ.

BACKGROUND: The electric organ of Tetronarce californica (an electric ray formerly known as Torpedo californica) is a classic preparation for biochemical studies of cholinergic neurotransmission. To broaden the usefulness of this preparation, we have performed a transcriptome assembly of the presynaptic component of the electric organ (the electric lobe). We combined our assembled transcriptome with a previous transcriptome of the postsynaptic electric organ, to define a MetaProteome containing pre- and post-synaptic components of the electric organ. RESULTS: Sequencing yielded 102 million paired-end 100 bp reads. De novo Trinity assembly was performed at Kmer 25 (default) and Kmers 27, 29, and 31. Trinity, generated around 103,000 transcripts, and 78,000 genes per assembly. Assemblies were evaluated based on the number of bases/transcripts assembled, RSEM-EVAL scores and informational content and completeness. We found that different assemblies scored differently according to the evaluation criteria used, and that while each individual assembly contained unique information, much of the assembly information was shared by all assemblies. To generate the presynaptic transcriptome (electric lobe), while capturing all information, assemblies were first clustered and then combined with postsynaptic transcripts (electric organ) downloaded from NCBI. The completness of the resulting clustered predicted MetaProteome was rigorously evaluated by comparing its information against the predicted proteomes from Homo sapiens, Callorhinchus milli, and the Transporter Classification Database (TCDB). CONCLUSIONS: In summary, we obtained a MetaProteome containing 92%, 88.5%, and 66% of the expected set of ultra-conserved sequences (i.e., BUSCOs), expected to be found for Eukaryotes, Metazoa, and Vertebrata, respectively. We cross-annotated the conserved set of proteins shared between the T. californica MetaProteome and the proteomes of H. sapiens and C. milli, using the H. sapiens genome as a reference. This information was used to predict the position in human pathways of the conserved members of the T. californica MetaProteome. We found proteins not detected before in T. californica, corresponding to processes involved in synaptic vesicle biology. Finally, we identified 42 transporter proteins in TCDB that were detected by the T. californica MetaProteome (electric fish) and not selected by a control proteome consisting of the combined proteomes of 12 widely diverse non-electric fishes by Reverse-Blast-Hit Blast. Combined, the information provided here is not only a unique tool for the study of cholinergic neurotransmission, but it is also a starting point for understanding the evolution of early vertebrates.

Additive neurogenesis supported by multiple stem cell populations mediates adult spinal cord development: A spatiotemporal statistical mapping analysis in a teleost model of indeterminate growth.

The knifefish Apteronotus leptorhynchus exhibits indeterminate growth throughout adulthood. This phenomenon extends to the spinal cord, presumably through the continuous addition of new neurons and glial cells. However, little is known about the developmental dynamics of cells added during adult growth. The present work characterizes the structural and functional development of the adult spinal cord in this model organism through a comprehensive quantitative analysis of the spatial and temporal dynamics of new cells at various developmental stages. This analysis, based on a novel statistical mapping approach, revealed within the adult spinal cord a wide distribution of both mitotically active and quiescent Sox2-expressing stem/progenitor cells (SPCs). While such cells are particularly concentrated within the ependymal layer near the central canal, the majority of them reside in the parenchyma, resembling the distribution of SPCs observed in the mammalian spinal cord. The active SPCs in the adult knifefish spinal cord give rise to transit amplifying progenitor cells that undergo a few additional mitotic divisions before developing into Hu C/D+ neurons and S100+ glial cells. There is no evidence of long-distance migration of the newborn cells. The persistence of cell proliferation and differentiation, combined with low levels of apoptosis, leads to a continuous addition of cells to the existing tissue. Newly generated neurons have functional and behavioral relevance, as indicated by the integration of axons of new electromotor neurons into the electric organ of these weakly electric fish. This results in a gradual increase in the amplitude of the electric organ discharge during adult development. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 77: 1269-1307, 2017.

A quest for excitation: Theoretical arguments and immunohistochemical evidence of excitatory granular cells in the ELL of Gnathonemus petersii.

The Electrosensory Lateral Line lobe (ELL) is the first central target where the electrosensory information encoded in the spatiotemporal pattern electroreceptor afferent discharges is processed. These afferents encode the minute amplitude changes of the basal electric field through both a change in latency and discharge rate. In the ELL the time and rate-coded input pattern of the sensory periphery goes through the granular cell layer before reaching the main efferent cells of the network: large fusiform (LF) and large ganglion (LG) cells. The evidence until now shows that granular cells are inhibitory. Given that large fusiform cells are excited by the sensory input, it remains a mystery how the afferent input produce excitation through a layer composed by only inhibitory cells. We addressed this problem by modeling how the known circuitry of the ELL could produce excitation in LF cells with only inhibitory granular cells. Alternatively we show that a network composed of a mix of excitatory and inhibitory granular cell not only performs better, as expected, carrying excitation to LF cells but it does so robustly and at higher sensitivity by enhancing the contrast of the electric image between the periphery and the ELLs output. We then show with refined histological methods that a subpopulation of the granular cells indeed are excitatory, providing the necessary input for this contrast enhancing mechanism.

Sternopygus macrurus electric organ transcriptome and cell size exhibit insensitivity to short-term electrical inactivity.

Electrical activity is an important regulator of cellular function and gene expression in electrically excitable cell types. In the weakly electric teleost fish Sternopygus macrurus, electrocytes, i.e., the current-producing cells of the electric organ, derive from a striated muscle lineage. Mature electrocytes are larger than muscle fibers, do not contain sarcomeres, and are driven continuously at frequencies higher than those exerted on muscle cells. Previous work showed that the removal of electrical activity by spinal cord transection (ST) for two and five weeks led to an upregulation of some sarcomeric proteins and a decrease in electrocyte size. To test whether changes in gene transcription preceded these phenotypic changes, we determined the sensitivity of electrocyte gene expression to electrical inactivity periods of two and five days after ST. Whole tissue gene expression profiles using deep RNA sequencing showed minimal alterations in the levels of myogenic transcription factor and sarcomeric transcripts after either ST period. Moreover, while analysis of differentially expressed genes showed a transient upregulation of genes associated with proteolytic mechanisms at two days and an increase in mRNA levels of cytoskeletal genes at five days after electrical silencing, electrocyte size was not affected. Electrical inactivity also resulted in the downregulation of genes that were classified into enriched clusters associated with functions of axon migration and synapse structure. Overall, these data demonstrate that unlike tissues in the myogenic lineage in other vertebrate species, regulation of gene transcription and cell size in the muscle-like electrocytes of S. macrurus is highly insensitive to short-term electrical inactivity. Moreover, together with data obtained from control and long-term ST studies, the present data suggest that neural input might influence post-transcriptional processes to affect the mature electrocyte phenotype.

Optimized Parallel Coding of Second-Order Stimulus Features by Heterogeneous Neural Populations.

UNLABELLED: Efficient processing of sensory input is essential to ensure an organism's survival in its natural environment. Growing evidence suggests that sensory neurons can optimally encode natural stimuli by ensuring that their tuning opposes stimulus statistics, such that the resulting neuronal response contains equal power at all frequencies (i.e., is "white"). Such temporal decorrelation or whitening has been observed across modalities, but the effects of neural heterogeneities on determining tuning and thus responses to natural stimuli have not been investigated. Here, we investigate how heterogeneities in sensory pyramidal neurons organized in three parallel maps representing the body surface determine responses to second-order electrosensory stimulus features in the weakly electric fish Apteronotus leptorhynchus While some sources of heterogeneities such as ON- and OFF-type responses to first-order did not affect responses to second-order electrosensory stimulus features, other sources of heterogeneity within and across the maps strongly determined responses. We found that these cells effectively performed a fractional differentiation operation on their input with exponents ranging from zero (no differentiation) to 0.4 (strong differentiation). Varying adaptation in a simple model explained these heterogeneities and predicted a strong correlation between fractional differentiation and adaptation. Using natural stimuli, we found that only a small fraction of neurons implemented temporal whitening. Rather, a large fraction of neurons did not perform any significant whitening and thus preserved natural input statistics in their responses. We propose that this information is needed to properly decode optimized information sent in parallel through temporally whitened responses based on context. SIGNIFICANCE STATEMENT: We demonstrate that heterogeneities in the same sensory neuron type can either have no or significant influence on their responses to second-order stimulus features. While an ON- or OFF-type response to first-order stimulus attributes has no significant influence on responses to second-order stimulus features, we found that only a small fraction of sensory neurons optimally encoded natural stimuli through high-pass filtering, thereby implementing temporal whitening. Surprisingly, a large fraction of sensory neurons performed little if no filtering of stimuli, thereby preserving natural stimulus statistics. We hypothesize that this pathway is necessary to properly decode optimized information contained in temporally whitened responses based on context.

Electrosensory processing in Apteronotus albifrons: implications for general and specific neural coding strategies across wave-type weakly electric fish species.

Understanding how the brain processes sensory input to generate behavior remains an important problem in neuroscience. Towards this end, it is useful to compare results obtained across multiple species to gain understanding as to the general principles of neural coding. Here we investigated hindbrain pyramidal cell activity in the weakly electric fish Apteronotus albifrons We found strong heterogeneities when looking at baseline activity. Additionally, ON- and OFF-type cells responded to increases and decreases of sinusoidal and noise stimuli, respectively. While both cell types displayed band-pass tuning, OFF-type cells were more broadly tuned than their ON-type counterparts. The observed heterogeneities in baseline activity as well as the greater broadband tuning of OFF-type cells were both similar to those previously reported in other weakly electric fish species, suggesting that they constitute general features of sensory processing. However, we found that peak tuning occurred at frequencies ∼15 Hz in A. albifrons, which is much lower than values reported in the closely related species Apteronotus leptorhynchus and the more distantly related species Eigenmannia virescens In response to stimuli with time-varying amplitude (i.e., envelope), ON- and OFF-type cells displayed similar high-pass tuning curves characteristic of fractional differentiation and possibly indicate optimized coding. These tuning curves were qualitatively similar to those of pyramidal cells in the closely related species A. leptorhynchus In conclusion, comparison between our and previous results reveals general and species-specific neural coding strategies. We hypothesize that differences in coding strategies, when observed, result from different stimulus distributions in the natural/social environment.

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.

Intragenus (Campylomormyrus) and intergenus hybrids in mormyrid fish: Physiological and histological investigations of the electric organ ontogeny.

African weakly electric mormyrid fish show a high diversity of their electric organ discharge (EOD) both across and within genera. Thanks to a recently developed technique of artificial reproduction in mormyrid fish, we were able to perform hybridizations between different genera and within one genus (Campylomormyrus). The hybrids of intergenus hybridizations exhibited different degrees of reduced survival related to the phylogenetic distance of the parent species: hybrids of the crosses between C. rhynchophorus and its sister genus Gnathonemus survived and developed normally. Hybrids between C. rhynchophorus and a Mormyrus species (a more basal clade compared to Campylomormyrus s) survived up to 42days and developed many malformations, e.g., at the level of the unpaired fins. Hybrids between C. numenius and Hippopotamyrus pictus (a derived clade, only distantly related to Campylomormyrus) only survived for two days during embryological development. Eight different hybrid combinations among five Campylomormyrus species (C. tamandua, C. compressirostris, C. tshokwe, C. rhynchophorus, C. numenius) were performed. The aim of the hybridizations was to combine species with (1) either caudal or rostral position of the main stalk innervating the electrocytes in the electric organ and (2) short, median or long duration of their EOD. The hybrids, though they are still juveniles, show very interesting features concerning electrocyte geometry as well as EOD form and duration: the caudal position of the stalk is prevailing over the rostral position, and the penetration of the stalk is dominant over the non-penetrating feature (in the Campylomormyrus hybrids); in the hybrid between C. rhynchophorus and Gnathonemus petersii it is the opposite. When crossing species with long and short EODs, it is always the long duration EOD that is expressed in the hybrids. The F1-Hybrids of the cross C. tamandua×C. compressirostris are fertile: viable F2-fish could be obtained with artificial reproduction.

A highly polarized excitable cell separates sodium channels from sodium-activated potassium channels by more than a millimeter.

The bioelectrical properties and resulting metabolic demands of electrogenic cells are determined by their morphology and the subcellular localization of ion channels. The electric organ cells (electrocytes) of the electric fish Eigenmannia virescens generate action potentials (APs) with Na(+) currents >10 µA and repolarize the AP with Na(+)-activated K(+) (KNa) channels. To better understand the role of morphology and ion channel localization in determining the metabolic cost of electrocyte APs, we used two-photon three-dimensional imaging to determine the fine cellular morphology and immunohistochemistry to localize the electrocytes' ion channels, ionotropic receptors, and Na(+)-K(+)-ATPases. We found that electrocytes are highly polarized cells ∼ 1.5 mm in anterior-posterior length and ∼ 0.6 mm in diameter, containing ∼ 30,000 nuclei along the cell periphery. The cell's innervated posterior region is deeply invaginated and vascularized with complex ultrastructural features, whereas the anterior region is relatively smooth. Cholinergic receptors and Na(+) channels are restricted to the innervated posterior region, whereas inward rectifier K(+) channels and the KNa channels that terminate the electrocyte AP are localized to the anterior region, separated by >1 mm from the only sources of Na(+) influx. In other systems, submicrometer spatial coupling of Na(+) and KNa channels is necessary for KNa channel activation. However, our computational simulations showed that KNa channels at a great distance from Na(+) influx can still terminate the AP, suggesting that KNa channels can be activated by distant sources of Na(+) influx and overturning a long-standing assumption that AP-generating ion channels are restricted to the electrocyte's posterior face.

Coding of envelopes by correlated but not single-neuron activity requires neural variability.

Understanding how the brain processes sensory information is often complicated by the fact that neurons exhibit trial-to-trial variability in their responses to stimuli. Indeed, the role of variability in sensory coding is still highly debated. Here, we examined how variability influences neural responses to naturalistic stimuli consisting of a fast time-varying waveform (i.e., carrier or first order) whose amplitude (i.e., envelope or second order) varies more slowly. Recordings were made from fish electrosensory and monkey vestibular sensory neurons. In both systems, we show that correlated but not single-neuron activity can provide detailed information about second-order stimulus features. Using a simple mathematical model, we made the strong prediction that such correlation-based coding of envelopes requires neural variability. Strikingly, the performance of correlated activity at predicting the envelope was similarly optimally tuned to a nonzero level of variability in both systems, thereby confirming this prediction. Finally, we show that second-order sensory information can only be decoded if one takes into account joint statistics when combining neural activities. Our results thus show that correlated but not single-neural activity can transmit information about the envelope, that such transmission requires neural variability, and that this information can be decoded. We suggest that envelope coding by correlated activity is a general feature of sensory processing that will be found across species and systems.

Nonhuman genetics. Genomic basis for the convergent evolution of electric organs.

Little is known about the genetic basis of convergent traits that originate repeatedly over broad taxonomic scales. The myogenic electric organ has evolved six times in fishes to produce electric fields used in communication, navigation, predation, or defense. We have examined the genomic basis of the convergent anatomical and physiological origins of these organs by assembling the genome of the electric eel (Electrophorus electricus) and sequencing electric organ and skeletal muscle transcriptomes from three lineages that have independently evolved electric organs. Our results indicate that, despite millions of years of evolution and large differences in the morphology of electric organ cells, independent lineages have leveraged similar transcription factors and developmental and cellular pathways in the evolution of electric organs.

Ionic mechanisms of microsecond-scale spike timing in single cells.

Electric fish image their environments and communicate by generating electric organ discharges through the simultaneous action potentials (APs) of electric organ cells (electrocytes) in the periphery. Steatogenys elegans generates a biphasic electrocyte discharge by the precisely regulated timing and waveform of APs generated from two excitable membranes present in each electrocyte. Current-clamp recordings of electrocyte APs reveal that the posterior membrane fires first, followed ∼30 µs later by an AP on the anterior membrane. This delay was maintained even as the onset of the first AP was advanced >5 ms by increasing stimulus intensity and across multiple spikes during bursts of APs elicited by prolonged stimulation. Simultaneous cell-attached loose-patch recordings of Na(+) currents on each membrane revealed that activation voltage for Na(+) channels on the posterior membrane was 10 mV hyperpolarized compared with Na(+) channels on the anterior membrane, with no differences in activation or inactivation kinetics. Computational simulations of electrocyte APs demonstrated that this difference in Na(+) current activation voltage was sufficient to maintain the proper firing order and the interspike delay. A similar difference in activation threshold has been reported for the Na(+) currents of the axon initial segment compared with somatic Na(+) channels of pyramidal neurons, suggesting convergent evolution of spike initiation and timing mechanisms across different systems of excitable cells.

A neural code for looming and receding motion is distributed over a population of electrosensory ON and OFF contrast cells.

Object saliency is based on the relative local-to-background contrast in the physical signals that underlie perceptual experience. As such, contrast-detecting neurons (ON/OFF cells) are found in many sensory systems, responding respectively to increased or decreased intensity within their receptive field centers. This differential sensitivity suggests that ON and OFF cells initiate segregated streams of information for positive and negative sensory contrast. However, while recording in vivo from the ON and OFF cells of Apteronotus leptorhynchus, we report that the reversal of stimulus motion triggers paradoxical responses to electrosensory contrast. By considering the instantaneous firing rates of both ON and OFF cell populations, a bidirectionally symmetric representation of motion is achieved for both positive and negative contrast stimuli. Whereas the firing rates of the individual contrast detecting neurons convey scalar information, such as object distance, it is their sequential activation over longer timescales that track changes in the direction of movement.

Statistics of the electrosensory input in the freely swimming weakly electric fish Apteronotus leptorhynchus.

The neural computations underlying sensory-guided behaviors can best be understood in view of the sensory stimuli to be processed under natural conditions. This input is often actively shaped by the movements of the animal and its sensory receptors. Little is known about natural sensory scene statistics taking into account the concomitant movement of sensory receptors in freely moving animals. South American weakly electric fish use a self-generated quasi-sinusoidal electric field for electrolocation and electrocommunication. Thousands of cutaneous electroreceptors detect changes in the transdermal potential (TDP) as the fish interact with conspecifics and the environment. Despite substantial knowledge about the circuitry and physiology of the electrosensory system, the statistical properties of the electrosensory input evoked by natural swimming movements have never been measured directly. Using underwater wireless telemetry, we recorded the TDP of Apteronotus leptorhynchus as they swam freely by themselves and during interaction with a conspecific. Swimming movements caused low-frequency TDP amplitude modulations (AMs). Interacting with a conspecific caused additional AMs around the difference frequency of their electric fields, with the amplitude of the AMs (envelope) varying at low frequencies due to mutual movements. Both AMs and envelopes showed a power-law relationship with frequency, indicating spectral scale invariance. Combining a computational model of the electric field with video tracking of movements, we show that specific swimming patterns cause characteristic spatiotemporal sensory input correlations that contain information that may be used by the brain to guide behavior.

Sexual dimorphism of the electrosensory system: a quantitative analysis of nerve axons in the dorsal anterior lateral line nerve of the blue-spotted Fantail Stingray (Taeniura lymma).

Quantitative studies of sensory axons provide invaluable insights into the functional significance and relative importance of a particular sensory modality. Despite the important role electroreception plays in the behaviour of elasmobranchs, to date, there have been no studies that have assessed the number of electrosensory axons that project from the peripheral ampullae to the central nervous system (CNS). The complex arrangement and morphology of the peripheral electrosensory system has a significant influence on its function. However, it is not sufficient to base conclusions about function on the peripheral system alone. To fully appreciate the function of the electrosensory system, it is essential to also assess the neural network that connects the peripheral system to the CNS. Using stereological techniques, unbiased estimates of the total number of axons were obtained for both the electrosensory bundles exiting individual ampullary organs and those entering the CNS (via the dorsal root of the anterior lateral line nerve, ALLN) in males and females of different sizes. The dorsal root of the ALLN consists solely of myelinated electrosensory axons and shows both ontogenetic and sexual dimorphism. In particular, females exhibit a greater abundance of electrosensory axons, which may result in improved sensitivity of the electrosensory system and may facilitate mate identification for reproduction. Also presented are detailed morphological data on the peripheral electrosensory system to allow a complete interpretation of the functional significance of the sexual dimorphism found in the ALLN.