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Electrosensory Midbrain Neurons Display Feature Invariant Responses to Natural Communication Stimuli.

Aumentado-Armstrong T, Metzen MG, Sproule MK, Chacron MJ - PLoS Comput. Biol. (2015)

Bottom Line: Such invariant responses were not seen in hindbrain electrosensory neurons providing afferent input to these midbrain neurons, suggesting that response invariance results from nonlinear integration of such input.We found that multiple combinations of parameter values could give rise to invariant responses matching those seen experimentally.Our model thus shows that there are multiple solutions towards achieving invariant responses and reveals how subthreshold membrane conductances help promote robust and invariant firing in response to heterogeneous stimulus waveforms associated with behaviorally relevant stimuli.

View Article: PubMed Central - PubMed

Affiliation: School of Computer Science, McGill University, Montreal, Quebec, Canada.

ABSTRACT
Neurons that respond selectively but in an invariant manner to a given feature of natural stimuli have been observed across species and systems. Such responses emerge in higher brain areas, thereby suggesting that they occur by integrating afferent input. However, the mechanisms by which such integration occurs are poorly understood. Here we show that midbrain electrosensory neurons can respond selectively and in an invariant manner to heterogeneity in behaviorally relevant stimulus waveforms. Such invariant responses were not seen in hindbrain electrosensory neurons providing afferent input to these midbrain neurons, suggesting that response invariance results from nonlinear integration of such input. To test this hypothesis, we built a model based on the Hodgkin-Huxley formalism that received realistic afferent input. We found that multiple combinations of parameter values could give rise to invariant responses matching those seen experimentally. Our model thus shows that there are multiple solutions towards achieving invariant responses and reveals how subthreshold membrane conductances help promote robust and invariant firing in response to heterogeneous stimulus waveforms associated with behaviorally relevant stimuli. We discuss the implications of our findings for the electrosensory and other systems.

No MeSH data available.


Natural electrocommunication stimuli display heterogeneous waveforms.A) Two weakly electric fish with their electric organ discharges (EODs) and a communication signal (“chirp”) from the emitter fish (green) to the receiver fish (blue). B) Schematic showing the EODs of the emitter and receiver (middle) fish as a function of time as well as the instantaneous EOD frequencies (top). The chirp consists of a transient increase in the emitter fish’s EOD frequency while the receiver fish’s frequency remains constant. The compound signal (bottom, gray) then consists of a beat resulting from the interference between the two quasi-sinusoidal EOD waveforms and the chirp then leads to a brief interruption in the beat. Note that the actual stimulus is the AM of the compound signal (bottom, black). C) Example waveforms resulting from natural chirping behavior. Note the large heterogeneities in the waveforms associated with the small (top) but not big chirps (bottom). D) Probability distribution of the similarity measure for big and small chirps. E) Chirp stimuli occur on all phases of the beat with uniform probability density but have fixed durations.
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pcbi.1004430.g001: Natural electrocommunication stimuli display heterogeneous waveforms.A) Two weakly electric fish with their electric organ discharges (EODs) and a communication signal (“chirp”) from the emitter fish (green) to the receiver fish (blue). B) Schematic showing the EODs of the emitter and receiver (middle) fish as a function of time as well as the instantaneous EOD frequencies (top). The chirp consists of a transient increase in the emitter fish’s EOD frequency while the receiver fish’s frequency remains constant. The compound signal (bottom, gray) then consists of a beat resulting from the interference between the two quasi-sinusoidal EOD waveforms and the chirp then leads to a brief interruption in the beat. Note that the actual stimulus is the AM of the compound signal (bottom, black). C) Example waveforms resulting from natural chirping behavior. Note the large heterogeneities in the waveforms associated with the small (top) but not big chirps (bottom). D) Probability distribution of the similarity measure for big and small chirps. E) Chirp stimuli occur on all phases of the beat with uniform probability density but have fixed durations.

Mentions: Our study focuses on how the electrosensory system of weakly electric fish can give rise to invariant neural responses to heterogeneous waveforms associated with natural electrocommunication stimuli. Such stimuli occur during interactions between two individual fish (Fig 1A). Because each individual fish has a different EOD frequency, interaction between the quasi-sinusoidal waveforms gives rise to a beat (Fig 1B, black trace in bottom panel) [22, 25]. Electrocommunication stimuli (i.e. “chirps”) consist of a brief (<40 ms) increase in the emitter fish’s EOD frequency (Fig 1B, green trace in top panel) while the EOD frequency of the receiver fish remains constant (Fig 1B, blue trace in top panel). Chirps have been traditionally segregated into type I (“big”) and type II (“small”): big chirps consist of a large increase in frequency (>150 Hz) accompanied by a decrease in the emitter fish’s EOD amplitude and tend to occur for large (>30 Hz) beat frequencies while small chirps instead consist mostly of a smaller (>30 Hz and <150 Hz) increase in the EOD frequency of the emitter fish that tend to occur for small (<30 Hz) beat frequencies [22, 23, 33].


Electrosensory Midbrain Neurons Display Feature Invariant Responses to Natural Communication Stimuli.

Aumentado-Armstrong T, Metzen MG, Sproule MK, Chacron MJ - PLoS Comput. Biol. (2015)

Natural electrocommunication stimuli display heterogeneous waveforms.A) Two weakly electric fish with their electric organ discharges (EODs) and a communication signal (“chirp”) from the emitter fish (green) to the receiver fish (blue). B) Schematic showing the EODs of the emitter and receiver (middle) fish as a function of time as well as the instantaneous EOD frequencies (top). The chirp consists of a transient increase in the emitter fish’s EOD frequency while the receiver fish’s frequency remains constant. The compound signal (bottom, gray) then consists of a beat resulting from the interference between the two quasi-sinusoidal EOD waveforms and the chirp then leads to a brief interruption in the beat. Note that the actual stimulus is the AM of the compound signal (bottom, black). C) Example waveforms resulting from natural chirping behavior. Note the large heterogeneities in the waveforms associated with the small (top) but not big chirps (bottom). D) Probability distribution of the similarity measure for big and small chirps. E) Chirp stimuli occur on all phases of the beat with uniform probability density but have fixed durations.
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Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4608831&req=5

pcbi.1004430.g001: Natural electrocommunication stimuli display heterogeneous waveforms.A) Two weakly electric fish with their electric organ discharges (EODs) and a communication signal (“chirp”) from the emitter fish (green) to the receiver fish (blue). B) Schematic showing the EODs of the emitter and receiver (middle) fish as a function of time as well as the instantaneous EOD frequencies (top). The chirp consists of a transient increase in the emitter fish’s EOD frequency while the receiver fish’s frequency remains constant. The compound signal (bottom, gray) then consists of a beat resulting from the interference between the two quasi-sinusoidal EOD waveforms and the chirp then leads to a brief interruption in the beat. Note that the actual stimulus is the AM of the compound signal (bottom, black). C) Example waveforms resulting from natural chirping behavior. Note the large heterogeneities in the waveforms associated with the small (top) but not big chirps (bottom). D) Probability distribution of the similarity measure for big and small chirps. E) Chirp stimuli occur on all phases of the beat with uniform probability density but have fixed durations.
Mentions: Our study focuses on how the electrosensory system of weakly electric fish can give rise to invariant neural responses to heterogeneous waveforms associated with natural electrocommunication stimuli. Such stimuli occur during interactions between two individual fish (Fig 1A). Because each individual fish has a different EOD frequency, interaction between the quasi-sinusoidal waveforms gives rise to a beat (Fig 1B, black trace in bottom panel) [22, 25]. Electrocommunication stimuli (i.e. “chirps”) consist of a brief (<40 ms) increase in the emitter fish’s EOD frequency (Fig 1B, green trace in top panel) while the EOD frequency of the receiver fish remains constant (Fig 1B, blue trace in top panel). Chirps have been traditionally segregated into type I (“big”) and type II (“small”): big chirps consist of a large increase in frequency (>150 Hz) accompanied by a decrease in the emitter fish’s EOD amplitude and tend to occur for large (>30 Hz) beat frequencies while small chirps instead consist mostly of a smaller (>30 Hz and <150 Hz) increase in the EOD frequency of the emitter fish that tend to occur for small (<30 Hz) beat frequencies [22, 23, 33].

Bottom Line: Such invariant responses were not seen in hindbrain electrosensory neurons providing afferent input to these midbrain neurons, suggesting that response invariance results from nonlinear integration of such input.We found that multiple combinations of parameter values could give rise to invariant responses matching those seen experimentally.Our model thus shows that there are multiple solutions towards achieving invariant responses and reveals how subthreshold membrane conductances help promote robust and invariant firing in response to heterogeneous stimulus waveforms associated with behaviorally relevant stimuli.

View Article: PubMed Central - PubMed

Affiliation: School of Computer Science, McGill University, Montreal, Quebec, Canada.

ABSTRACT
Neurons that respond selectively but in an invariant manner to a given feature of natural stimuli have been observed across species and systems. Such responses emerge in higher brain areas, thereby suggesting that they occur by integrating afferent input. However, the mechanisms by which such integration occurs are poorly understood. Here we show that midbrain electrosensory neurons can respond selectively and in an invariant manner to heterogeneity in behaviorally relevant stimulus waveforms. Such invariant responses were not seen in hindbrain electrosensory neurons providing afferent input to these midbrain neurons, suggesting that response invariance results from nonlinear integration of such input. To test this hypothesis, we built a model based on the Hodgkin-Huxley formalism that received realistic afferent input. We found that multiple combinations of parameter values could give rise to invariant responses matching those seen experimentally. Our model thus shows that there are multiple solutions towards achieving invariant responses and reveals how subthreshold membrane conductances help promote robust and invariant firing in response to heterogeneous stimulus waveforms associated with behaviorally relevant stimuli. We discuss the implications of our findings for the electrosensory and other systems.

No MeSH data available.