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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.


Hindbrain electrosensory neurons projecting to midbrain do not 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 hindbrain region Electrosensory lateral line lobe (ELL). B,C) Responses of example ON and OFF-type ELL pyramidal neurons to different chirp stimuli (black), respectively. 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 different responses to chirps as a given cell responds sometimes with excitation and sometimes with inhibition. D) Population-averaged VPD (left), CSI (middle), and FI (right) values for ELL ON, OFF-cells, and TS neurons. “*” indicates statistical significance at the p = 0.05 level using a one-way ANOVA. Values for ON, OFF, and TS cells, respectively, are VPD = 53.3±5.3, 46.8±3.4, 7.4±1.9; CSI = -0.05±0.02, -0.03±0.04, 0.61±0.08; FI = 0.00±0.00, 0.004±0.004, 0.536±0.093. E) FI values obtained from the population-averaged responses for ON-cells, OFF-cells, and ON+OFF-cells are also shown and are all much lower than FI values obtained for TS neurons.
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pcbi.1004430.g003: Hindbrain electrosensory neurons projecting to midbrain do not 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 hindbrain region Electrosensory lateral line lobe (ELL). B,C) Responses of example ON and OFF-type ELL pyramidal neurons to different chirp stimuli (black), respectively. 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 different responses to chirps as a given cell responds sometimes with excitation and sometimes with inhibition. D) Population-averaged VPD (left), CSI (middle), and FI (right) values for ELL ON, OFF-cells, and TS neurons. “*” indicates statistical significance at the p = 0.05 level using a one-way ANOVA. Values for ON, OFF, and TS cells, respectively, are VPD = 53.3±5.3, 46.8±3.4, 7.4±1.9; CSI = -0.05±0.02, -0.03±0.04, 0.61±0.08; FI = 0.00±0.00, 0.004±0.004, 0.536±0.093. E) FI values obtained from the population-averaged responses for ON-cells, OFF-cells, and ON+OFF-cells are also shown and are all much lower than FI values obtained for TS neurons.

Mentions: Perhaps the simplest potential explanation for the experimentally observed invariant responses of TS neurons described above is that they are simply inherited from their afferent ELL pyramidal neurons. Previous studies have found two types of ELL pyramidal neurons [36]: ON-type neurons respond with excitation while OFF-type neurons instead respond with inhibition to increases in EOD amplitude, respectively. We thus recorded ELL pyramidal neuron responses to the same stimuli presented to TS neurons (Fig 3A). In contrast to TS neurons and consistent with previous results [37], ON (n = 25) and OFF-type (n = 20) ELL pyramidal cells displayed pronounced responses to the beat in the form of phase locking (Fig 3B and 3C). Although ON and OFF-type ELL pyramidal cells also responded to all chirp waveforms, they did not do so in an invariant manner as they were excited by some chirp waveforms but inhibited by others (Fig 3B and 3C). We quantified the responses of ON and OFF-type ELL pyramidal cells to chirps using CSI, VPD, and FI. Overall, both ON and OFF-type ELL neurons displayed significantly smaller CSI values than TS neurons (Fig 3D, left) indicating that they tended to respond to both the beat and the chirp, consistent with previous findings [30–32]. Moreover, there were significantly greater differences between the responses of ON and OFF-type ELL neurons to different chirp waveforms as compared to that of TS neurons (Fig 3D, middle). Therefore, the responses of TS neurons to chirps were significantly more invariant than those of ELL neurons (ON: 0.000±0.000, OFF: 0.004±0.004, TS: 0.54±0.09, one-way ANOVA with Tukey-Kramer correction, p<0.05) (Fig 3D, right). We conclude that the feature invariant responses observed in TS are not simply inherited from ELL neurons and must rather result from TS neurons integrating such input.


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

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

Hindbrain electrosensory neurons projecting to midbrain do not 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 hindbrain region Electrosensory lateral line lobe (ELL). B,C) Responses of example ON and OFF-type ELL pyramidal neurons to different chirp stimuli (black), respectively. 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 different responses to chirps as a given cell responds sometimes with excitation and sometimes with inhibition. D) Population-averaged VPD (left), CSI (middle), and FI (right) values for ELL ON, OFF-cells, and TS neurons. “*” indicates statistical significance at the p = 0.05 level using a one-way ANOVA. Values for ON, OFF, and TS cells, respectively, are VPD = 53.3±5.3, 46.8±3.4, 7.4±1.9; CSI = -0.05±0.02, -0.03±0.04, 0.61±0.08; FI = 0.00±0.00, 0.004±0.004, 0.536±0.093. E) FI values obtained from the population-averaged responses for ON-cells, OFF-cells, and ON+OFF-cells are also shown and are all much lower than FI values obtained for TS neurons.
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pcbi.1004430.g003: Hindbrain electrosensory neurons projecting to midbrain do not 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 hindbrain region Electrosensory lateral line lobe (ELL). B,C) Responses of example ON and OFF-type ELL pyramidal neurons to different chirp stimuli (black), respectively. 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 different responses to chirps as a given cell responds sometimes with excitation and sometimes with inhibition. D) Population-averaged VPD (left), CSI (middle), and FI (right) values for ELL ON, OFF-cells, and TS neurons. “*” indicates statistical significance at the p = 0.05 level using a one-way ANOVA. Values for ON, OFF, and TS cells, respectively, are VPD = 53.3±5.3, 46.8±3.4, 7.4±1.9; CSI = -0.05±0.02, -0.03±0.04, 0.61±0.08; FI = 0.00±0.00, 0.004±0.004, 0.536±0.093. E) FI values obtained from the population-averaged responses for ON-cells, OFF-cells, and ON+OFF-cells are also shown and are all much lower than FI values obtained for TS neurons.
Mentions: Perhaps the simplest potential explanation for the experimentally observed invariant responses of TS neurons described above is that they are simply inherited from their afferent ELL pyramidal neurons. Previous studies have found two types of ELL pyramidal neurons [36]: ON-type neurons respond with excitation while OFF-type neurons instead respond with inhibition to increases in EOD amplitude, respectively. We thus recorded ELL pyramidal neuron responses to the same stimuli presented to TS neurons (Fig 3A). In contrast to TS neurons and consistent with previous results [37], ON (n = 25) and OFF-type (n = 20) ELL pyramidal cells displayed pronounced responses to the beat in the form of phase locking (Fig 3B and 3C). Although ON and OFF-type ELL pyramidal cells also responded to all chirp waveforms, they did not do so in an invariant manner as they were excited by some chirp waveforms but inhibited by others (Fig 3B and 3C). We quantified the responses of ON and OFF-type ELL pyramidal cells to chirps using CSI, VPD, and FI. Overall, both ON and OFF-type ELL neurons displayed significantly smaller CSI values than TS neurons (Fig 3D, left) indicating that they tended to respond to both the beat and the chirp, consistent with previous findings [30–32]. Moreover, there were significantly greater differences between the responses of ON and OFF-type ELL neurons to different chirp waveforms as compared to that of TS neurons (Fig 3D, middle). Therefore, the responses of TS neurons to chirps were significantly more invariant than those of ELL neurons (ON: 0.000±0.000, OFF: 0.004±0.004, TS: 0.54±0.09, one-way ANOVA with Tukey-Kramer correction, p<0.05) (Fig 3D, right). We conclude that the feature invariant responses observed in TS are not simply inherited from ELL neurons and must rather result from TS neurons integrating such input.

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.