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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.


Widely different combinations of parameter values give rise to feature invariant responses in our model.Five example model neurons and their responses to the different chirp stimuli. The FI values for models 1 to 5 were 0.90, 0.79, 0.91, 0.77, and 0.89, respectively. Parameter values for models 1 to 5 where σB = 0.42, 0.41, 0.35, 0.40, 0.42; Ibias = -9.4, -6.6, -18.1, -5.2, -6.5 nA; gsyn = 0.10, 0.13, 0.16, 0.10, 0.09 μS; gh = 0.24, 0, 0.48, 0.02, 0 μS; gT = 2.10, 0, 3.99, 0, 5.6 μS. Other parameter values were the same as that indicated in the methods.
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pcbi.1004430.g005: Widely different combinations of parameter values give rise to feature invariant responses in our model.Five example model neurons and their responses to the different chirp stimuli. The FI values for models 1 to 5 were 0.90, 0.79, 0.91, 0.77, and 0.89, respectively. Parameter values for models 1 to 5 where σB = 0.42, 0.41, 0.35, 0.40, 0.42; Ibias = -9.4, -6.6, -18.1, -5.2, -6.5 nA; gsyn = 0.10, 0.13, 0.16, 0.10, 0.09 μS; gh = 0.24, 0, 0.48, 0.02, 0 μS; gT = 2.10, 0, 3.99, 0, 5.6 μS. Other parameter values were the same as that indicated in the methods.

Mentions: This algorithm identified multiple sets of physiologically realistic parameter values that all gave rise to feature invariant responses that matched those seen experimentally. Fig 5 shows five such examples. For each set of parameter values, the model neuron responded to each chirp with 1–4 action potentials, as seen experimentally, in a similar fashion as quantified by similar FI scores despite having different parameter values. Importantly, we had both T- and h-type conductances set to zero (i.e. gT = gh = 0 μS) for model 2 indicating that these subthreshold membrane conductances are not necessary to observe feature invariance. Thus, our model predicts that the spiking nonlinearity is sufficient to produce feature invariant responses to natural electrocommunication stimuli.


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

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

Widely different combinations of parameter values give rise to feature invariant responses in our model.Five example model neurons and their responses to the different chirp stimuli. The FI values for models 1 to 5 were 0.90, 0.79, 0.91, 0.77, and 0.89, respectively. Parameter values for models 1 to 5 where σB = 0.42, 0.41, 0.35, 0.40, 0.42; Ibias = -9.4, -6.6, -18.1, -5.2, -6.5 nA; gsyn = 0.10, 0.13, 0.16, 0.10, 0.09 μS; gh = 0.24, 0, 0.48, 0.02, 0 μS; gT = 2.10, 0, 3.99, 0, 5.6 μS. Other parameter values were the same as that indicated in the methods.
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getmorefigures.php?uid=PMC4608831&req=5

pcbi.1004430.g005: Widely different combinations of parameter values give rise to feature invariant responses in our model.Five example model neurons and their responses to the different chirp stimuli. The FI values for models 1 to 5 were 0.90, 0.79, 0.91, 0.77, and 0.89, respectively. Parameter values for models 1 to 5 where σB = 0.42, 0.41, 0.35, 0.40, 0.42; Ibias = -9.4, -6.6, -18.1, -5.2, -6.5 nA; gsyn = 0.10, 0.13, 0.16, 0.10, 0.09 μS; gh = 0.24, 0, 0.48, 0.02, 0 μS; gT = 2.10, 0, 3.99, 0, 5.6 μS. Other parameter values were the same as that indicated in the methods.
Mentions: This algorithm identified multiple sets of physiologically realistic parameter values that all gave rise to feature invariant responses that matched those seen experimentally. Fig 5 shows five such examples. For each set of parameter values, the model neuron responded to each chirp with 1–4 action potentials, as seen experimentally, in a similar fashion as quantified by similar FI scores despite having different parameter values. Importantly, we had both T- and h-type conductances set to zero (i.e. gT = gh = 0 μS) for model 2 indicating that these subthreshold membrane conductances are not necessary to observe feature invariance. Thus, our model predicts that the spiking nonlinearity is sufficient to produce feature invariant responses to natural electrocommunication stimuli.

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.