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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.


Related in: MedlinePlus

Midbrain electrosensory neurons display feature invariant responses to natural electrocommunication stimuli.A) Schematic showing a fish with stimulation electrodes on each side as well as a recording electrode from the midbrain region Torus semicircularis (TS). B) Responses of an example TS neuron to different chirp stimuli (black). The blue dots mark the occurrence of action potentials to 20 repeated presentations of the stimulus waveform (raster plot) and the red curve shows the firing rate response averaged over trials (PSTH). Note the similarity in the response to each waveform as the neuron fires at the chirp onset with one-two spikes in each case.
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pcbi.1004430.g002: Midbrain electrosensory neurons display feature invariant responses to natural electrocommunication stimuli.A) Schematic showing a fish with stimulation electrodes on each side as well as a recording electrode from the midbrain region Torus semicircularis (TS). B) Responses of an example TS neuron to different chirp stimuli (black). The blue dots mark the occurrence of action potentials to 20 repeated presentations of the stimulus waveform (raster plot) and the red curve shows the firing rate response averaged over trials (PSTH). Note the similarity in the response to each waveform as the neuron fires at the chirp onset with one-two spikes in each case.

Mentions: We next investigated whether electrosensory midbrain neurons responded to big and small chirps in a feature invariant manner. To do so, we recorded the responses of TS neurons (N = 137) (Fig 2A) to both small and big chirp stimuli that captured the relatively heterogeneous waveforms seen for the former and the relatively homogeneous waveforms seen for the latter (Fig 2B). Previous studies have found that TS neurons either do not respond selectively or respond selectively but differentially to different chirp stimulus waveforms [32]. Here we focused on neurons that responded selectively to the chirp stimulus and not the beat and whose responses to different chirp waveforms were similar (see Methods). We found that some TS neurons in our dataset (N = 9) responded selectively to both small and big chirp stimuli but in a similar manner through silence during the beat and by the firing of 1–2 action potentials at a short latency (~15 ms) after the chirp onset (Fig 2B). We quantified whether the response was selective to the chirp waveform using the chirp selectivity index (CSI) as done previously [32] (see Methods) and we quantified differences between spiking responses to different chirp waveforms using the Victor-Purpura distance metric (VPD) [35] (see Methods). We obtained CSI = 1 and VPD = 1.19 for the example neuron shown in Fig 2. We also computed a feature invariance index (FI) score that captured a neuron’s ability to respond selectively but invariantly to chirps. We obtained FI = 0.99 for the example neuron shown in Fig 2.


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

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

Midbrain electrosensory neurons display feature invariant responses to natural electrocommunication stimuli.A) Schematic showing a fish with stimulation electrodes on each side as well as a recording electrode from the midbrain region Torus semicircularis (TS). B) Responses of an example TS neuron to different chirp stimuli (black). The blue dots mark the occurrence of action potentials to 20 repeated presentations of the stimulus waveform (raster plot) and the red curve shows the firing rate response averaged over trials (PSTH). Note the similarity in the response to each waveform as the neuron fires at the chirp onset with one-two spikes in each case.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4608831&req=5

pcbi.1004430.g002: Midbrain electrosensory neurons display feature invariant responses to natural electrocommunication stimuli.A) Schematic showing a fish with stimulation electrodes on each side as well as a recording electrode from the midbrain region Torus semicircularis (TS). B) Responses of an example TS neuron to different chirp stimuli (black). The blue dots mark the occurrence of action potentials to 20 repeated presentations of the stimulus waveform (raster plot) and the red curve shows the firing rate response averaged over trials (PSTH). Note the similarity in the response to each waveform as the neuron fires at the chirp onset with one-two spikes in each case.
Mentions: We next investigated whether electrosensory midbrain neurons responded to big and small chirps in a feature invariant manner. To do so, we recorded the responses of TS neurons (N = 137) (Fig 2A) to both small and big chirp stimuli that captured the relatively heterogeneous waveforms seen for the former and the relatively homogeneous waveforms seen for the latter (Fig 2B). Previous studies have found that TS neurons either do not respond selectively or respond selectively but differentially to different chirp stimulus waveforms [32]. Here we focused on neurons that responded selectively to the chirp stimulus and not the beat and whose responses to different chirp waveforms were similar (see Methods). We found that some TS neurons in our dataset (N = 9) responded selectively to both small and big chirp stimuli but in a similar manner through silence during the beat and by the firing of 1–2 action potentials at a short latency (~15 ms) after the chirp onset (Fig 2B). We quantified whether the response was selective to the chirp waveform using the chirp selectivity index (CSI) as done previously [32] (see Methods) and we quantified differences between spiking responses to different chirp waveforms using the Victor-Purpura distance metric (VPD) [35] (see Methods). We obtained CSI = 1 and VPD = 1.19 for the example neuron shown in Fig 2. We also computed a feature invariance index (FI) score that captured a neuron’s ability to respond selectively but invariantly to chirps. We obtained FI = 0.99 for the example neuron shown in Fig 2.

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.


Related in: MedlinePlus