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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.


Modeling TS neuron responses to natural electrocommunication stimuli.Our model consists of summing the population-averaged responses of ON and OFF-type ELL pyramidal neurons with weights σB and 1-σB, respectively, and giving the resulting signal as synaptic input to a model TS neuron that includes various membrane conductances that were modeled using the Hodgkin-Huxley formalism: leak gleak, spiking sodium gNa, delayed rectifier potassium gK, T-type calcium gT, hyperpolarization activated inward rectifier gh.
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pcbi.1004430.g004: Modeling TS neuron responses to natural electrocommunication stimuli.Our model consists of summing the population-averaged responses of ON and OFF-type ELL pyramidal neurons with weights σB and 1-σB, respectively, and giving the resulting signal as synaptic input to a model TS neuron that includes various membrane conductances that were modeled using the Hodgkin-Huxley formalism: leak gleak, spiking sodium gNa, delayed rectifier potassium gK, T-type calcium gT, hyperpolarization activated inward rectifier gh.

Mentions: To investigate whether, and if so how, nonlinear integration of ELL input by TS neurons is sufficient to observe feature invariant responses to chirp stimuli, we built a model TS neuron based on the Hodgkin-Huxley formalism that included different membrane conductances seen experimentally in TS neurons (Fig 4). Importantly, the afferent ELL input to the model was the weighted sum of the population-averaged experimentally observed responses of ON and OFF-type pyramidal neurons to chirp stimuli convolved with an alpha function to mimic synaptic input (see Methods). Model parameters were similar to those used in previous modeling studies of TS neurons [38–40] or varied systematically. We then used a constrained differential evolution algorithm to identify combinations of parameter values that gave rise to the highest feature invariant responses as quantified by FI (see Methods).


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

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

Modeling TS neuron responses to natural electrocommunication stimuli.Our model consists of summing the population-averaged responses of ON and OFF-type ELL pyramidal neurons with weights σB and 1-σB, respectively, and giving the resulting signal as synaptic input to a model TS neuron that includes various membrane conductances that were modeled using the Hodgkin-Huxley formalism: leak gleak, spiking sodium gNa, delayed rectifier potassium gK, T-type calcium gT, hyperpolarization activated inward rectifier gh.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi.1004430.g004: Modeling TS neuron responses to natural electrocommunication stimuli.Our model consists of summing the population-averaged responses of ON and OFF-type ELL pyramidal neurons with weights σB and 1-σB, respectively, and giving the resulting signal as synaptic input to a model TS neuron that includes various membrane conductances that were modeled using the Hodgkin-Huxley formalism: leak gleak, spiking sodium gNa, delayed rectifier potassium gK, T-type calcium gT, hyperpolarization activated inward rectifier gh.
Mentions: To investigate whether, and if so how, nonlinear integration of ELL input by TS neurons is sufficient to observe feature invariant responses to chirp stimuli, we built a model TS neuron based on the Hodgkin-Huxley formalism that included different membrane conductances seen experimentally in TS neurons (Fig 4). Importantly, the afferent ELL input to the model was the weighted sum of the population-averaged experimentally observed responses of ON and OFF-type pyramidal neurons to chirp stimuli convolved with an alpha function to mimic synaptic input (see Methods). Model parameters were similar to those used in previous modeling studies of TS neurons [38–40] or varied systematically. We then used a constrained differential evolution algorithm to identify combinations of parameter values that gave rise to the highest feature invariant responses as quantified by FI (see Methods).

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.