Cellular and circuit properties supporting different sensory coding strategies in electric fish and other systems

2012 ◽  
Vol 22 (4) ◽  
pp. 686-692 ◽  
Author(s):  
Gary Marsat ◽  
André Longtin ◽  
Leonard Maler
Keyword(s):  
Electric Fish ◽  
Sensory Coding ◽  
Coding Strategies

Sensory coding and corollary discharge effects in mormyrid electric fish

1989 ◽  
Vol 146 (1) ◽  
pp. 229-253 ◽  
Author(s):  
C. C. Bell
Keyword(s):  
Electric Fish ◽  
Spatial Information ◽  
Electric Organ Discharge ◽  
Low Frequency ◽  
Electric Organ ◽  
Motor Command ◽  
Corollary Discharge ◽  
Weakly Electric Fish ◽  
Central Projection ◽  
Sensory Coding

Weakly electric fish use their electrosensory systems for electrocommunication, active electrolocation and low-frequency passive electrolocation. In electric fish of the family Mormyridae, these three purposes are mediated by separate classes of electroreceptors: electrocommunication by Knollenorgan electroreceptors, active electrolocation by Mormyromast electroreceptors and low-frequency passive electrolocation by ampullary electroreceptors. The primary afferent fibres from each class of electroreceptors terminate in a separate central region. Thus, the mormyrid electrosensory system has three anatomically and functionally distinct subsystems. This review describes the sensory coding and initial processing in each of the three subsystems, with an emphasis on the Knollenorgan and Mormyromast subsystems. The Knollenorgan subsystem is specialized for the measurement of temporal information but appears to ignore both intensity and spatial information. In contrast, the Mormyromast subsystem is specialized for the measurement of both intensity and spatial information. The morphological and physiological characteristics of the primary afferents and their central projection regions are quite different for the two subsystems and reflect the type of information which the subsystems preserve. This review also describes the electric organ corollary discharge (EOCD) effects which are present in the central projection regions of each of the three electrosensory subsystems. These EOCD effects are driven by the motor command that drives the electric organ to discharge. The EOCD effects are different in each of the three subsystems and these differences reflect differences in both the pattern and significance of the sensory information that is evoked by the fish's own electric organ discharge. Some of the EOCD effects are invariant, whereas others are plastic and depend on previous afferent input. The mormyrid work is placed within two general contexts: (a) the measurement of time and intensity in sensory systems, and (b) the various roles of motor command (efferent) signals and self-induced sensory (reafferent) signals in sensorimotor systems.

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

2016 ◽  
Vol 116 (6) ◽  
pp. 2909-2921 ◽  
Author(s):  
Diana Martinez ◽  
Michael G. Metzen ◽  
Maurice J. Chacron
Keyword(s):  
Fish Species ◽  
Related Species ◽  
Neural Coding ◽  
Electric Fish ◽  
Weakly Electric Fish ◽  
Closely Related Species ◽  
Tuning Curves ◽  
Baseline Activity ◽  
Coding Strategies ◽  
Weakly Electric

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.

scholarly journals Task-specific sensory coding strategies matched to detection and discrimination behaviors in Apteronotus leptorhynchus

2017 ◽  
Author(s):  
K.M. Allen ◽  
G. Marsat
Keyword(s):  
General Principle ◽  
Neural Coding ◽  
Sensory Systems ◽  
Model Systems ◽  
Behavioral Performance ◽  
Sensory Coding ◽  
Apteronotus Leptorhynchus ◽  
Neural Codes ◽  
Coding Strategies ◽  
Behavioral Tasks

ABSTRACTAll sensory systems must reliably translate information about the environment into a neural code, mediating perception. The most relevant aspects of stimuli may change as behavioral context changes, making efficient encoding of information more challenging. Sensory systems must balance rapid detection of a stimulus with perception of fine details that enable discrimination between similar stimuli. We show that in a species of weakly electric fish, Apteronotus leptorhynchus, two coding strategies are employed for these separate behavioral tasks. Using communication signals produced in different contexts, we demonstrate a strong correlation between neural coding strategies and behavioral performance on a discrimination task. Extracellular recordings of pyramidal cells within the electrosensory lateral line lobe of alert fish show two distinct response patterns, either burst discharges with little variation between different signals of the same category, or a graded, heterogeneous response that contains enough information to discriminate between signals with slight variations. When faced with a discrimination-based task, the behavioral performance of the fish closely matches predictions based on coding strategy. Comparisons of these results with neural and behavioral responses observed in other model systems suggest that our study highlights a general principle in the way different neural codes are utilized in the sensory system.SIGNIFICANCE STATEMENTResearch relating the structure of stimuli to the response of sensory neurons has left us with a detailed understanding of how different neural codes can represent information. Although various aspects of neural responses have been related to perceptual abilities, general principles relating behavioral tasks to sensory coding strategies are lacking. A major distinction can be made between signals that must simply be detected versus stimuli that must also be finely discriminated and evaluated. We show that these two different perceptual tasks are systematically matched by distinct neural coding strategies and we argue that our study identifies a general principle that is observed in various sensory systems.Conflict of interest statementThe authors declare no competing financial interests.

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
Keyword(s):  
Central Nervous System ◽  
Nervous System ◽  
Related Species ◽  
Electric Fish ◽  
Weakly Electric Fish ◽  
Closely Related Species ◽  
Communication Signals ◽  
Coding Strategies ◽  
The Central Nervous System ◽  
Weakly Electric

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.

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