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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.


Changes in neural sensitivity caused by pharmacologically manipulating SK channels cause predictable changes in behavioural responses.(a) Schematic representation showing how changes in the neural tuning characterized by exponent αneuron are predicted to cause changes in behavioural sensitivity characterized by exponent αbehaviour. (b) Schematic representation of the bilateral ELL drug injection setup by which UCL or EBIO is injected simultaneously in both ELL's on each side of the brain via two electrodes. (c) Population-averaged normalized behavioural sensitivities 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 αbehaviour given in the figure. Inset: population-averaged αbehaviour values under control (red), after UCL application (purple) and after EBIO application (cyan). (d) Population-averaged matching index between behavioural response and natural stimulus statistics under control (red), after UCL application (purple) (N=6), and after EBIO application (cyan) (N=6). Both drugs significantly decreased the matching index value. (e) Actual (solid) and predicted (striped) changes in exponent αbehaviour caused by UCL (purple) and EBIO (cyan) application. The changes were predicted solely from the changes in neural tuning exponent αneuron shown in Fig. 6d. ‘**' and ‘*' indicate statistical significance a using a one-way ANOVA with post hoc Bonferroni correction at the P=0.01 and 0.05 levels, respectively.
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f8: Changes in neural sensitivity caused by pharmacologically manipulating SK channels cause predictable changes in behavioural responses.(a) Schematic representation showing how changes in the neural tuning characterized by exponent αneuron are predicted to cause changes in behavioural sensitivity characterized by exponent αbehaviour. (b) Schematic representation of the bilateral ELL drug injection setup by which UCL or EBIO is injected simultaneously in both ELL's on each side of the brain via two electrodes. (c) Population-averaged normalized behavioural sensitivities 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 αbehaviour given in the figure. Inset: population-averaged αbehaviour values under control (red), after UCL application (purple) and after EBIO application (cyan). (d) Population-averaged matching index between behavioural response and natural stimulus statistics under control (red), after UCL application (purple) (N=6), and after EBIO application (cyan) (N=6). Both drugs significantly decreased the matching index value. (e) Actual (solid) and predicted (striped) changes in exponent αbehaviour caused by UCL (purple) and EBIO (cyan) application. The changes were predicted solely from the changes in neural tuning exponent αneuron shown in Fig. 6d. ‘**' and ‘*' indicate statistical significance a using a one-way ANOVA with post hoc Bonferroni correction at the P=0.01 and 0.05 levels, respectively.

Mentions: We hypothesized that behavioural sensitivity is directly related to ELL pyramidal neuron tuning. Thus, changing the neural tuning exponent αneuron should cause changes in the behavioural exponent αbehaviour (Fig. 8a) and a simple model predicts that Δαbehaviour=−Δαneuron (see Methods). To test our hypothesis, we injected UCL and EBIO bilaterally into the ELL (Fig. 8b)4244 (see Methods). As a control, injection of saline alone had no significant effect on behavioural responses (Supplementary Fig. 3). In contrast, UCL and EBIO injection both strongly altered behavioural sensitivity (Fig. 8c). Indeed, behavioural sensitivity decreased more steeply following UCL application as quantified by a greater behavioural exponent αbehaviour (Fig. 8c, compare red and purple, Fig. 8c, inset). In contrast, behavioural sensitivity decreased less steeply after EBIO application as quantified by a lesser behavioural exponent αbehaviour (Fig. 8c, compare red and cyan, Fig. 8c, inset). Importantly, behavioural sensitivity was no longer matched to natural stimulus statistics after both UCL and EBIO application (Fig. 8d). Consistent with our simple model, changes in behavioural tuning αbehaviour following the UCL and the EBIO applications were consistent with predictions made from changes in αneuron (Fig. 8e). Thus, we conclude that efficient processing of natural envelope stimuli by ELL pyramidal neurons does indeed ensure that behavioural sensitivity at the organismal level is matched to natural stimulus statistics.


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

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

Changes in neural sensitivity caused by pharmacologically manipulating SK channels cause predictable changes in behavioural responses.(a) Schematic representation showing how changes in the neural tuning characterized by exponent αneuron are predicted to cause changes in behavioural sensitivity characterized by exponent αbehaviour. (b) Schematic representation of the bilateral ELL drug injection setup by which UCL or EBIO is injected simultaneously in both ELL's on each side of the brain via two electrodes. (c) Population-averaged normalized behavioural sensitivities 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 αbehaviour given in the figure. Inset: population-averaged αbehaviour values under control (red), after UCL application (purple) and after EBIO application (cyan). (d) Population-averaged matching index between behavioural response and natural stimulus statistics under control (red), after UCL application (purple) (N=6), and after EBIO application (cyan) (N=6). Both drugs significantly decreased the matching index value. (e) Actual (solid) and predicted (striped) changes in exponent αbehaviour caused by UCL (purple) and EBIO (cyan) application. The changes were predicted solely from the changes in neural tuning exponent αneuron shown in Fig. 6d. ‘**' and ‘*' indicate statistical significance a using a one-way ANOVA with post hoc Bonferroni correction at the P=0.01 and 0.05 levels, respectively.
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f8: Changes in neural sensitivity caused by pharmacologically manipulating SK channels cause predictable changes in behavioural responses.(a) Schematic representation showing how changes in the neural tuning characterized by exponent αneuron are predicted to cause changes in behavioural sensitivity characterized by exponent αbehaviour. (b) Schematic representation of the bilateral ELL drug injection setup by which UCL or EBIO is injected simultaneously in both ELL's on each side of the brain via two electrodes. (c) Population-averaged normalized behavioural sensitivities 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 αbehaviour given in the figure. Inset: population-averaged αbehaviour values under control (red), after UCL application (purple) and after EBIO application (cyan). (d) Population-averaged matching index between behavioural response and natural stimulus statistics under control (red), after UCL application (purple) (N=6), and after EBIO application (cyan) (N=6). Both drugs significantly decreased the matching index value. (e) Actual (solid) and predicted (striped) changes in exponent αbehaviour caused by UCL (purple) and EBIO (cyan) application. The changes were predicted solely from the changes in neural tuning exponent αneuron shown in Fig. 6d. ‘**' and ‘*' indicate statistical significance a using a one-way ANOVA with post hoc Bonferroni correction at the P=0.01 and 0.05 levels, respectively.
Mentions: We hypothesized that behavioural sensitivity is directly related to ELL pyramidal neuron tuning. Thus, changing the neural tuning exponent αneuron should cause changes in the behavioural exponent αbehaviour (Fig. 8a) and a simple model predicts that Δαbehaviour=−Δαneuron (see Methods). To test our hypothesis, we injected UCL and EBIO bilaterally into the ELL (Fig. 8b)4244 (see Methods). As a control, injection of saline alone had no significant effect on behavioural responses (Supplementary Fig. 3). In contrast, UCL and EBIO injection both strongly altered behavioural sensitivity (Fig. 8c). Indeed, behavioural sensitivity decreased more steeply following UCL application as quantified by a greater behavioural exponent αbehaviour (Fig. 8c, compare red and purple, Fig. 8c, inset). In contrast, behavioural sensitivity decreased less steeply after EBIO application as quantified by a lesser behavioural exponent αbehaviour (Fig. 8c, compare red and cyan, Fig. 8c, inset). Importantly, behavioural sensitivity was no longer matched to natural stimulus statistics after both UCL and EBIO application (Fig. 8d). Consistent with our simple model, changes in behavioural tuning αbehaviour following the UCL and the EBIO applications were consistent with predictions made from changes in αneuron (Fig. 8e). Thus, we conclude that efficient processing of natural envelope stimuli by ELL pyramidal neurons does indeed ensure that behavioural sensitivity at the organismal level is matched to natural stimulus statistics.

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.