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Temporal decorrelation by SK channels enables efficient neural coding and perception of natural stimuli.

Huang CG, Zhang ZD, Chacron MJ - Nat Commun (2016)

Bottom Line: However, the mechanisms by which such efficient processing is achieved, and the consequences for perception and behaviour remain poorly understood.Specifically, these channels allow for the high-pass filtering of sensory input, thereby removing temporal correlations or, equivalently, whitening frequency response power.Our results thus demonstrate a novel mechanism by which the nervous system can implement efficient processing and perception of natural sensory input that is likely to be shared across systems and species.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, McGill University, 3655 Sir William Osler, Montreal, Quebec, Canada H3G 1Y6.

ABSTRACT
It is commonly assumed that neural systems efficiently process natural sensory input. However, the mechanisms by which such efficient processing is achieved, and the consequences for perception and behaviour remain poorly understood. Here we show that small conductance calcium-activated potassium (SK) channels enable efficient neural processing and perception of natural stimuli. Specifically, these channels allow for the high-pass filtering of sensory input, thereby removing temporal correlations or, equivalently, whitening frequency response power. Varying the degree of adaptation through pharmacological manipulation of SK channels reduced efficiency of coding of natural stimuli, which in turn gave rise to predictable changes in behavioural responses that were no longer matched to natural stimulus statistics. Our results thus demonstrate a novel mechanism by which the nervous system can implement efficient processing and perception of natural sensory input that is likely to be shared across systems and species.

No MeSH data available.


Pharmacological inactivation and activation of SK channels alter neural sensitivity and both reduce coding efficiency of natural stimuli.(a) Schematic representation showing how a double-barrel electrode approaches and can eject glutamate as well as either UCL (SK channel antagonist) or EBIO (SK channel agonist) in the near vicinity of the pyramidal neuron being recorded from. (b) Normalized gain as a function of frequency obtained for sinusoidal stimuli under control (red), after UCL application (purple) and after EBIO application (cyan). The circles show the experimental data and the dashed lines the best power law fits with exponents αneuron given in the figure. UCL and EBIO application decreased and increased the steepness of the curve, respectively (black arrows). (c) Response power spectra to natural stimuli under control (solid red), after UCL application (solid purple) and after EBIO application (solid cyan). The dashed lines show the predicted values obtained from the power law fits in b. UCL and EBIO application led to response power spectra that were no longer independent of frequency (black arrows). (d) Population-averaged neural exponent αneuron under control (red), after UCL application (purple) (N=6), and after EBIO application (cyan) (N=8). (e) Population-averaged white index values under control (red), after UCL application (purple) (N=6), and after EBIO application (cyan) (N=8). ‘**' indicates statistical significance at the P=0.01 level using a one-way ANOVA with post hoc Bonferroni correction.
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f6: Pharmacological inactivation and activation of SK channels alter neural sensitivity and both reduce coding efficiency of natural stimuli.(a) Schematic representation showing how a double-barrel electrode approaches and can eject glutamate as well as either UCL (SK channel antagonist) or EBIO (SK channel agonist) in the near vicinity of the pyramidal neuron being recorded from. (b) Normalized gain as a function of frequency obtained for sinusoidal stimuli under control (red), after UCL application (purple) and after EBIO application (cyan). The circles show the experimental data and the dashed lines the best power law fits with exponents αneuron given in the figure. UCL and EBIO application decreased and increased the steepness of the curve, respectively (black arrows). (c) Response power spectra to natural stimuli under control (solid red), after UCL application (solid purple) and after EBIO application (solid cyan). The dashed lines show the predicted values obtained from the power law fits in b. UCL and EBIO application led to response power spectra that were no longer independent of frequency (black arrows). (d) Population-averaged neural exponent αneuron under control (red), after UCL application (purple) (N=6), and after EBIO application (cyan) (N=8). (e) Population-averaged white index values under control (red), after UCL application (purple) (N=6), and after EBIO application (cyan) (N=8). ‘**' indicates statistical significance at the P=0.01 level using a one-way ANOVA with post hoc Bonferroni correction.

Mentions: We focused on small conductance calcium-activated potassium (SK) channels. This is because previous results have shown that pharmacologically activating and inactivating these currents will increase and decrease adaptation in ELL pyramidal neurons, respectively3940. We thus hypothesized that pharmacological activation and inactivation of SK channels will increase and decrease fractional differentiation by pyramidal neurons, respectively, thereby altering tuning. Both manipulations are then predicted to decrease efficient coding of natural stimuli by temporal whitening. We thus micro-injected the SK channel antagonist UCL-1684 (UCL) as well as the SK channel agonist 1-EBIO (EBIO) in the ELL using well-established methodology (Bastian41; Deemyad et al.42; Supplementary Fig. 2A, see Methods) (Fig. 6a). We note that previous studies have shown that injection of saline alone using this methodology does not alter pyramidal neuron activity4142. Consistent with previous results3943, we found that UCL and EBIO application both strongly altered pyramidal neuron activity in the absence of stimulation (Supplementary Figs 2B–D).


Temporal decorrelation by SK channels enables efficient neural coding and perception of natural stimuli.

Huang CG, Zhang ZD, Chacron MJ - Nat Commun (2016)

Pharmacological inactivation and activation of SK channels alter neural sensitivity and both reduce coding efficiency of natural stimuli.(a) Schematic representation showing how a double-barrel electrode approaches and can eject glutamate as well as either UCL (SK channel antagonist) or EBIO (SK channel agonist) in the near vicinity of the pyramidal neuron being recorded from. (b) Normalized gain as a function of frequency obtained for sinusoidal stimuli under control (red), after UCL application (purple) and after EBIO application (cyan). The circles show the experimental data and the dashed lines the best power law fits with exponents αneuron given in the figure. UCL and EBIO application decreased and increased the steepness of the curve, respectively (black arrows). (c) Response power spectra to natural stimuli under control (solid red), after UCL application (solid purple) and after EBIO application (solid cyan). The dashed lines show the predicted values obtained from the power law fits in b. UCL and EBIO application led to response power spectra that were no longer independent of frequency (black arrows). (d) Population-averaged neural exponent αneuron under control (red), after UCL application (purple) (N=6), and after EBIO application (cyan) (N=8). (e) Population-averaged white index values under control (red), after UCL application (purple) (N=6), and after EBIO application (cyan) (N=8). ‘**' indicates statistical significance at the P=0.01 level using a one-way ANOVA with post hoc Bonferroni correction.
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f6: Pharmacological inactivation and activation of SK channels alter neural sensitivity and both reduce coding efficiency of natural stimuli.(a) Schematic representation showing how a double-barrel electrode approaches and can eject glutamate as well as either UCL (SK channel antagonist) or EBIO (SK channel agonist) in the near vicinity of the pyramidal neuron being recorded from. (b) Normalized gain as a function of frequency obtained for sinusoidal stimuli under control (red), after UCL application (purple) and after EBIO application (cyan). The circles show the experimental data and the dashed lines the best power law fits with exponents αneuron given in the figure. UCL and EBIO application decreased and increased the steepness of the curve, respectively (black arrows). (c) Response power spectra to natural stimuli under control (solid red), after UCL application (solid purple) and after EBIO application (solid cyan). The dashed lines show the predicted values obtained from the power law fits in b. UCL and EBIO application led to response power spectra that were no longer independent of frequency (black arrows). (d) Population-averaged neural exponent αneuron under control (red), after UCL application (purple) (N=6), and after EBIO application (cyan) (N=8). (e) Population-averaged white index values under control (red), after UCL application (purple) (N=6), and after EBIO application (cyan) (N=8). ‘**' indicates statistical significance at the P=0.01 level using a one-way ANOVA with post hoc Bonferroni correction.
Mentions: We focused on small conductance calcium-activated potassium (SK) channels. This is because previous results have shown that pharmacologically activating and inactivating these currents will increase and decrease adaptation in ELL pyramidal neurons, respectively3940. We thus hypothesized that pharmacological activation and inactivation of SK channels will increase and decrease fractional differentiation by pyramidal neurons, respectively, thereby altering tuning. Both manipulations are then predicted to decrease efficient coding of natural stimuli by temporal whitening. We thus micro-injected the SK channel antagonist UCL-1684 (UCL) as well as the SK channel agonist 1-EBIO (EBIO) in the ELL using well-established methodology (Bastian41; Deemyad et al.42; Supplementary Fig. 2A, see Methods) (Fig. 6a). We note that previous studies have shown that injection of saline alone using this methodology does not alter pyramidal neuron activity4142. Consistent with previous results3943, we found that UCL and EBIO application both strongly altered pyramidal neuron activity in the absence of stimulation (Supplementary Figs 2B–D).

Bottom Line: However, the mechanisms by which such efficient processing is achieved, and the consequences for perception and behaviour remain poorly understood.Specifically, these channels allow for the high-pass filtering of sensory input, thereby removing temporal correlations or, equivalently, whitening frequency response power.Our results thus demonstrate a novel mechanism by which the nervous system can implement efficient processing and perception of natural sensory input that is likely to be shared across systems and species.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, McGill University, 3655 Sir William Osler, Montreal, Quebec, Canada H3G 1Y6.

ABSTRACT
It is commonly assumed that neural systems efficiently process natural sensory input. However, the mechanisms by which such efficient processing is achieved, and the consequences for perception and behaviour remain poorly understood. Here we show that small conductance calcium-activated potassium (SK) channels enable efficient neural processing and perception of natural stimuli. Specifically, these channels allow for the high-pass filtering of sensory input, thereby removing temporal correlations or, equivalently, whitening frequency response power. Varying the degree of adaptation through pharmacological manipulation of SK channels reduced efficiency of coding of natural stimuli, which in turn gave rise to predictable changes in behavioural responses that were no longer matched to natural stimulus statistics. Our results thus demonstrate a novel mechanism by which the nervous system can implement efficient processing and perception of natural sensory input that is likely to be shared across systems and species.

No MeSH data available.