scholarly journals Stimulus background influences phase invariant coding by correlated neural activity

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Michael G Metzen ◽  
Maurice J Chacron

Previously we reported that correlations between the activities of peripheral afferents mediate a phase invariant representation of natural communication stimuli that is refined across successive processing stages thereby leading to perception and behavior in the weakly electric fish Apteronotus leptorhynchus (Metzen et al., 2016). Here, we explore how phase invariant coding and perception of natural communication stimuli are affected by changes in the sinusoidal background over which they occur. We found that increasing background frequency led to phase locking, which decreased both detectability and phase invariant coding. Correlated afferent activity was a much better predictor of behavior as assessed from both invariance and detectability than single neuron activity. Thus, our results provide not only further evidence that correlated activity likely determines perception of natural communication signals, but also a novel explanation as to why these preferentially occur on top of low frequency as well as low-intensity sinusoidal backgrounds.

2010 ◽  
Vol 104 (4) ◽  
pp. 1955-1968 ◽  
Author(s):  
J. Engelmann ◽  
S. Gertz ◽  
J. Goulet ◽  
A. Schuh ◽  
G. von der Emde

Weakly electric fish use electroreception for both active and passive electrolocation and for electrocommunication. While both active and passive electrolocation systems are prominent in weakly electric Mormyriform fishes, knowledge of their passive electrolocation ability is still scarce. To better estimate the contribution of passive electric sensing to the orientation toward electric stimuli in weakly electric fishes, we investigated frequency tuning applying classical input-output characterization and stimulus reconstruction methods to reveal the encoding capabilities of ampullary receptor afferents. Ampullary receptor afferents were most sensitive (threshold: 40 μV/cm) at low frequencies (<10 Hz) and appear to be tuned to a mix of amplitude and slope of the input signals. The low-frequency tuning was corroborated by behavioral experiments, but behavioral thresholds were one order of magnitude higher. The integration of simultaneously recorded afferents of similar frequency-tuning resulted in strongly enhanced signal-to-noise ratios and increased mutual information rates but did not increase the range of frequencies detectable by the system. Theoretically the neuronal integration of input from receptors experiencing opposite polarities of a stimulus (left and right side of the fish) was shown to enhance encoding of such stimuli, including an increase of bandwidth. Covariance and coherence analysis showed that spiking of ampullary afferents is sufficiently explained by the spike-triggered average, i.e., receptors respond to a single linear feature of the stimulus. Our data support the notion of a division of labor of the active and passive electrosensory systems in weakly electric fishes based on frequency tuning. Future experiments will address the role of central convergence of ampullary input that we expect to lead to higher sensitivity and encoding power of the system.


2010 ◽  
Vol 7 (2) ◽  
pp. 197-200 ◽  
Author(s):  
Vincent Fugère ◽  
Hernán Ortega ◽  
Rüdiger Krahe

Animals often use signals to communicate their dominance status and avoid the costs of combat. We investigated whether the frequency of the electric organ discharge (EOD) of the weakly electric fish, Sternarchorhynchus sp., signals the dominance status of individuals. We correlated EOD frequency with body size and found a strong positive relationship. We then performed a competition experiment in which we found that higher frequency individuals were dominant over lower frequency ones. Finally, we conducted an electrical playback experiment and found that subjects more readily approached and attacked the stimulus electrodes when they played low-frequency signals than high-frequency ones. We propose that EOD frequency communicates dominance status in this gymnotiform species.


2008 ◽  
Vol 99 (4) ◽  
pp. 1825-1835 ◽  
Author(s):  
Maurice J. Chacron ◽  
Joseph Bastian

Sensory stimuli typically activate many receptors at once and therefore should lead to increases in correlated activity among central neurons. Such correlated activity could be a critical feature in the encoding and decoding of information in central circuits. Here we characterize correlated activity in response to two biologically relevant classes of sensory stimuli in the primary electrosensory nuclei, the electrosensory lateral line lobe, of the weakly electric fish Apteronotus leptorhynchus. Our results show that these neurons can display significant correlations in their baseline activities that depend on the amount of receptive field overlap. A detailed analysis of spike trains revealed that correlated activity resulted predominantly from a tendency to fire synchronous or anti-synchronous bursts of spikes. We also explored how different stimulation protocols affected correlated activity: while prey-like stimuli increased correlated activity, conspecific-like stimuli decreased correlated activity. We also computed the correlations between the variabilities of each neuron to repeated presentations of the same stimulus (noise correlations) and found lower amounts of noise correlation for communication stimuli. Therefore the decrease in correlated activity seen with communication stimuli is caused at least in part by reduced noise correlations. This differential modulation in correlated activity occurred because of changes in burst firing at the individual neuron level. Our results show that different categories of behaviorally relevant input will differentially affect correlated activity. In particular, we show that the number of correlated bursts within a given time window could be used by postsynaptic neurons to distinguish between both stimulus categories.


2009 ◽  
Vol 102 (2) ◽  
pp. 714-723 ◽  
Author(s):  
Gary Marsat ◽  
Rémi D. Proville ◽  
Leonard Maler

It is an important task in neuroscience to find general principles that relate neural codes to the structure of the signals they encode. The structure of sensory signals can be described in many ways, but one important categorization distinguishes continuous from transient signals. We used the communication signals of the weakly electric fish to reveal how transient signals (chirps) can be easily distinguished from the continuous signal they disrupt. These communication signals—low-frequency sinusoids interrupted by high-frequency transients—were presented to pyramidal cells of the electrosensory lateral line lobe (ELL) during in vivo recordings. We show that a specific population of electrosensory neurons encodes the occurrence of the transient signal by synchronously producing a burst of spikes, whereas bursting was neither common nor synchronous in response to the continuous signal. We also confirmed that burst can be triggered by low-frequency modulations typical of prey signals. However, these bursts are more common in a different segment of the ELL and during spatially localized stimulation. These localized stimuli will elicit synchronized bursting only in a restricted number of cells the receptive fields of which overlap the spatial extent of the stimulus. Therefore the number of cells simultaneously producing a burst and the ELL segment responding most strongly may carry the information required to disambiguate chirps from prey signals. Finally we show that the burst response to chirps is due to a biophysical mechanism previously characterized by in vitro studies of electrosensory neurons. We conclude that bursting and synchrony across cells are important mechanisms used by sensory neurons to carry the information about behaviorally relevant but transient signals.


2018 ◽  
Vol 91 (4) ◽  
pp. 214-227
Author(s):  
Brandon Neeley ◽  
Tyler Overholt ◽  
Emily Artz ◽  
Steven G. Kinsey ◽  
Gary Marsat

Cannabinoid (CB) receptors are widespread in the nervous system and influence a variety of behaviors. Weakly electric fish have been a useful model system in the study of the neural basis of behavior, but we know nothing of the role played by the CB system. Here, we determine the overall behavioral effect of a nonselective CB receptor agonist, namely Δ9-tetrahydrocannabinol (THC), in the weakly electric fish Apte­ronotus leptorhynchus. Using various behavioral paradigms involving social stimuli, we show that THC decreases locomotor behavior, as in many species, and influences communication and social behavior. Across the different experiments, we found that the propensity to emit communication signals (chirps) and seek social interactions was affected in a context-dependent manner. We explicitly tested this hypothesis by comparing the behavioral effects of THC injection in fish placed in a novel versus a familiar social and physical environment. THC-injected fish were less likely to chirp than control fish in familiar situations but not in novel ones. The tendency to be in close proximity to other fish was affected only in novel environments, with control fish clustering more than THC-injected ones. By identifying behaviors affected by CB agonists, our study can guide further comparative and neurophysiological studies of the role of the CB system using a weakly electric fish as a model.


2018 ◽  
Author(s):  
K.M. Allen ◽  
G. Marsat

ABSTRACTAs communication signal properties change, through genetic drift or selective pressure, the sensory systems that receive these signals must also adapt to maintain sensitivity and adaptability in an array of contexts. Shedding light on this process helps us understand how sensory codes are tailored to specific tasks. In a species of weakly electric fish, Apteronotus albifrons, we examined the unique neurophysiological properties that support the encoding of electrosensory communication signals that the animal encounters in social exchanges. We compare our findings to known coding properties of the closely related species, Apteronotus leptorhynchus, to establish how these animals differ in their ability to encode their distinctive communication signals. While there are many similarities between these two species, we found notable differences leading to relatively poor coding of the details of chirp structure occurring on high-frequency background beats. As a result, small differences in chirp properties are poorly resolved by the nervous system. We performed behavioral tests to relate A. albifrons chirp coding strategies to its use of chirps during social encounters. Our results suggest that A. albifrons do not exchange frequent chirps in non-breeding condition, particularly when the beat frequency is high. These findings parallel the mediocre chirp coding accuracy in that they both point to a reduced reliance on frequent and rich exchange of information through chirps during these social interactions. Therefore, our study suggests that neural coding strategies in the central nervous system vary across species in a way that parallels the behavioral use of the sensory signals.SIGNIFICANCESender-receiver matching is a phenomenon commonly observed in the peripheral nervous system. It enables communication production and reception to evolve together so that conspecifics remain sensitive to important signals. In this manuscript we examine this phenomenon in the central nervous system of the weakly electric fish A. albifrons and compare its processing of communication signals to a closely related species (A. leptorhynchus). Although some differences across the two species can help tailor the system for processing species-specific signals, our data indicate that encoding of communication signals in A. albifrons is not as sensitive as in A. leptorhynchus for certain categories of signals. Our data support the idea that the extent of sender-receiver matching can vary as a function of behavioral needs.


2018 ◽  
Author(s):  
Brandon Neeley ◽  
Tyler Overholt ◽  
Emily Artz ◽  
Steven G Kinsey ◽  
Gary Marsat

AbstractCannabinoid (CB) receptors are widespread in the nervous system and influence a variety of behaviors. Weakly electric fish has been a useful model system in the study of the neural basis of behavior but we know nothing of the role played by the CB system. Here, we determine the overall behavioral effect of a CB receptor agonist (i.e., Δ9-tetrahydrocannabinol, THC) in the weakly electric fish A. leptorhynchus. Using various behavioral paradigms involving social stimuli, we show that THC decreases locomotor behavior as in many species and influences the communication and social behavior. Across the different experiments we found that the propensity to emit communication signals (chirps) and to seek social interactions was affected in a context-dependent manner. We explicitly tested this hypothesis by comparing the behavioral effects of THC injection in fish placed in a novel versus familiar social and physical environments. THC-injected fish were less likely to chirp than control in familiar situation but not in novel ones. The tendency to be in close proximity was affected only in novel environments whith control fish clustering more than THC-injected ones. By identifying behaviors affected by CB agonists, our study can guide further comparative and neurophysiological studies of the role of the CB system using weakly electric fish as a model.


eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Michael G Metzen ◽  
Volker Hofmann ◽  
Maurice J Chacron

Neural representations of behaviorally relevant stimulus features displaying invariance with respect to different contexts are essential for perception. However, the mechanisms mediating their emergence and subsequent refinement remain poorly understood in general. Here, we demonstrate that correlated neural activity allows for the emergence of an invariant representation of natural communication stimuli that is further refined across successive stages of processing in the weakly electric fish Apteronotus leptorhynchus. Importantly, different patterns of input resulting from the same natural communication stimulus occurring in different contexts all gave rise to similar behavioral responses. Our results thus reveal how a generic neural circuit performs an elegant computation that mediates the emergence and refinement of an invariant neural representation of natural stimuli that most likely constitutes a neural correlate of perception.


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