scholarly journals Neural processing of communication signals: The extent of sender-receiver matching varies across species of Apteronotus

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.

2016 ◽  
Vol 116 (6) ◽  
pp. 2909-2921 ◽  
Author(s):  
Diana Martinez ◽  
Michael G. Metzen ◽  
Maurice J. Chacron

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.


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.


1999 ◽  
Vol 202 (10) ◽  
pp. 1319-1326
Author(s):  
R.J. Dunn ◽  
D. Bottai ◽  
L. Maler

The complete sequences and expression patterns of the NR1 (aptNR1) subunit of the N-methyl-d-aspartate (NMDA) receptor and its alternative splice isoforms have been determined for the weakly electric fish Apteronotus leptorhynchus. The deduced amino acid sequence of aptNR1 is approximately 88 % identical to the NR1 sequences of other vertebrate. Two of the three alternative splice cassettes previously described for mammalian NR1s, N1 and C1, are present in aptNR1, but the third cassette, C2, is not found. In addition, two teleost-specific splice cassettes occur on the N-terminal side of the C1 sequence. The cellular patterns of aptNR1 expression, including the patterns of N1 and C1 splicing, have been mapped using the in situ hybridization technique. High levels of aptNR1 mRNA were detected throughout the central nervous system including most neurons of the electrosensory system, with the highest levels in electrosensory lateral line lobe pyramidal cells. Expression of the N1 splice isoform was higher in more caudal regions of the brain, and expression of the C1 splice isoform was higher in more rostral regions. The N1 splice isoform was present in almost all NR1-positive cells, in contrast to the C1 splice isoform which was restricted to a subset of NR1-positive cells. These results demonstrate that the NR1 subunit of the NMDA receptor is evolutionarily conserved across species and that regulation of alternative RNA splicing modulates the properties of NR1 in different neurons of the central nervous system of A. leptorhynchus.


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.


2021 ◽  
Author(s):  
Avner Wallach ◽  
Alexandre Melanson ◽  
Andre Longtin ◽  
Len Maler

Recent studies have shown that high-level neural activity often exhibits mixed selectivity to multi-variate signals. How such representations arise and how they modulate natural behavior is poorly understood. The social behavior of weakly electric fish is relatively low-dimensional and easily reproduced in the laboratory. Here we show how electrosensory signals related to courtship and rivalry in Apteronotus leptorhynchus are represented in the preglomerular nucleus, the thalamic region exclusively connecting the midbrain with the pallium. We show that preglomerular cells convert their midbrain inputs into a mixed selectivity code that includes corollary discharge of outgoing communication signals. We discuss how the preglomerular pallial targets might use these inputs to control social behavior and determine dominance in male-male competition and female mate selection during courtship. Our results showcase the potential of the electrocommunication system as an accessible model for studying the neural substrates of social behavior and principles of multi-dimensional neural representation.


2017 ◽  
Author(s):  
Jörg Henninger ◽  
Rüdiger Krahe ◽  
Frank Kirschbaum ◽  
Jan Grewe ◽  
Jan Benda

AbstractSensory systems evolve in the ecological niches each species is occupying. Accordingly, the tuning of sensory neurons is expected to be adapted to the statistics of natural stimuli. For an unbiased quantification of sensory scenes we tracked natural communication behavior of the weakly electric fish Apteronotus rostratus in their Neotropical rainforest habitat with high spatio-temporal resolution over several days. In the context of courtship and aggression we observed large quantities of electrocommunication signals. Echo responses and acknowledgment signals clearly demonstrated the behavioral relevance of these signals. The known tuning properties of peripheral electrosensory neurons suggest, however, that they are barely activated by these obviously relevant signals. Frequencies of courtship signals are clearly mismatched with the frequency tuning of neuronal population activity. Our results emphasize the importance of quantifying sensory scenes derived from freely behaving animals in their natural habitats for understanding the evolution and function of neural systems.


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