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Synaptic representation of locomotion in single cerebellar granule cells.

Powell K, Mathy A, Duguid I, Häusser M - Elife (2015)

Bottom Line: Here, we use in vivo patch-clamp recordings to show that locomotion can be directly read out from mossy fiber synaptic input and spike output in single granule cells.The increase in granule cell spiking during locomotion is enhanced by glutamate spillover currents recruited during movement.Thus, synaptic input delivers remarkably rich information to single neurons during locomotion.

View Article: PubMed Central - PubMed

Affiliation: Wolfson Institute for Biomedical Research and Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom.

ABSTRACT
The cerebellum plays a crucial role in the regulation of locomotion, but how movement is represented at the synaptic level is not known. Here, we use in vivo patch-clamp recordings to show that locomotion can be directly read out from mossy fiber synaptic input and spike output in single granule cells. The increase in granule cell spiking during locomotion is enhanced by glutamate spillover currents recruited during movement. Surprisingly, the entire step sequence can be predicted from input EPSCs and output spikes of a single granule cell, suggesting that a robust gait code is present already at the cerebellar input layer and transmitted via the granule cell pathway to downstream Purkinje cells. Thus, synaptic input delivers remarkably rich information to single neurons during locomotion.

No MeSH data available.


Related in: MedlinePlus

Spillover acts like a temporal filter.(A) We convolved the ESPCs rates with a biexponential trace to give a filtered trace. (B) The cross-correlation between the filtered traced and EPSCs resembles the cross-correlation between spillover and EPSCs (Figure 2C). (C) The step cycle modulation of the EPSCs is drastically reduced by the filtering procedure (from 0.30 ± 0.03 to 0.13 ± 0.2; p = 4.65 × 10−4; n = 18, 2 limbs for n = 9 cells).DOI:http://dx.doi.org/10.7554/eLife.07290.009
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fig4s1: Spillover acts like a temporal filter.(A) We convolved the ESPCs rates with a biexponential trace to give a filtered trace. (B) The cross-correlation between the filtered traced and EPSCs resembles the cross-correlation between spillover and EPSCs (Figure 2C). (C) The step cycle modulation of the EPSCs is drastically reduced by the filtering procedure (from 0.30 ± 0.03 to 0.13 ± 0.2; p = 4.65 × 10−4; n = 18, 2 limbs for n = 9 cells).DOI:http://dx.doi.org/10.7554/eLife.07290.009

Mentions: Next, we examined the relationship of activity parameters to the step cycle of the mouse, focusing on the two forelimbs. Animals initiated periods of locomotion spontaneously, and would often be still for several seconds between these periods. Electrophysiologically recorded parameters in mossy fiber boutons and granule cells were strikingly modulated by the step cycle (Figure 4A–C), in either or both of the forelimbs. Specifically, statistically significant step cycle modulations were observed for mossy fiber bouton spiking (3 out of 4 cells for the right limb, 1 out of 4 cells for the left limb), granule cell EPSCs (5 out of 9 for the right limb, 4 out of 9 cells for the left limb), and granule cell spiking (0 out of 7 for the right limb, 2 out of 7 cells for the left limb); while spillover was not significantly correlated with step cycle. In Figure 4—figure supplement 1, we show why it is possible that despite high cross-correlations between spillover and EPSCs, significant step cycle modulations are not seen: a temporally filtered EPSC trace (using a biexponential kernel with rise time = 50 ms and decay = 100 ms) exhibits a cross-correlation with the original trace which is similar to spillover (Figure 4—figure supplement 1B), however its step cycle modulations are significantly lower (from 0.30 ± 0.03 to 0.13 ± 0.2, p = 4.65 × 10−4, paired t-test; n = 18—that is, 2 limbs for n = 9 cells), due to the low-pass properties of the filter.10.7554/eLife.07290.008Figure 4.Decoding activity in a single granule cell can predict the step cycle.


Synaptic representation of locomotion in single cerebellar granule cells.

Powell K, Mathy A, Duguid I, Häusser M - Elife (2015)

Spillover acts like a temporal filter.(A) We convolved the ESPCs rates with a biexponential trace to give a filtered trace. (B) The cross-correlation between the filtered traced and EPSCs resembles the cross-correlation between spillover and EPSCs (Figure 2C). (C) The step cycle modulation of the EPSCs is drastically reduced by the filtering procedure (from 0.30 ± 0.03 to 0.13 ± 0.2; p = 4.65 × 10−4; n = 18, 2 limbs for n = 9 cells).DOI:http://dx.doi.org/10.7554/eLife.07290.009
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4499793&req=5

fig4s1: Spillover acts like a temporal filter.(A) We convolved the ESPCs rates with a biexponential trace to give a filtered trace. (B) The cross-correlation between the filtered traced and EPSCs resembles the cross-correlation between spillover and EPSCs (Figure 2C). (C) The step cycle modulation of the EPSCs is drastically reduced by the filtering procedure (from 0.30 ± 0.03 to 0.13 ± 0.2; p = 4.65 × 10−4; n = 18, 2 limbs for n = 9 cells).DOI:http://dx.doi.org/10.7554/eLife.07290.009
Mentions: Next, we examined the relationship of activity parameters to the step cycle of the mouse, focusing on the two forelimbs. Animals initiated periods of locomotion spontaneously, and would often be still for several seconds between these periods. Electrophysiologically recorded parameters in mossy fiber boutons and granule cells were strikingly modulated by the step cycle (Figure 4A–C), in either or both of the forelimbs. Specifically, statistically significant step cycle modulations were observed for mossy fiber bouton spiking (3 out of 4 cells for the right limb, 1 out of 4 cells for the left limb), granule cell EPSCs (5 out of 9 for the right limb, 4 out of 9 cells for the left limb), and granule cell spiking (0 out of 7 for the right limb, 2 out of 7 cells for the left limb); while spillover was not significantly correlated with step cycle. In Figure 4—figure supplement 1, we show why it is possible that despite high cross-correlations between spillover and EPSCs, significant step cycle modulations are not seen: a temporally filtered EPSC trace (using a biexponential kernel with rise time = 50 ms and decay = 100 ms) exhibits a cross-correlation with the original trace which is similar to spillover (Figure 4—figure supplement 1B), however its step cycle modulations are significantly lower (from 0.30 ± 0.03 to 0.13 ± 0.2, p = 4.65 × 10−4, paired t-test; n = 18—that is, 2 limbs for n = 9 cells), due to the low-pass properties of the filter.10.7554/eLife.07290.008Figure 4.Decoding activity in a single granule cell can predict the step cycle.

Bottom Line: Here, we use in vivo patch-clamp recordings to show that locomotion can be directly read out from mossy fiber synaptic input and spike output in single granule cells.The increase in granule cell spiking during locomotion is enhanced by glutamate spillover currents recruited during movement.Thus, synaptic input delivers remarkably rich information to single neurons during locomotion.

View Article: PubMed Central - PubMed

Affiliation: Wolfson Institute for Biomedical Research and Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom.

ABSTRACT
The cerebellum plays a crucial role in the regulation of locomotion, but how movement is represented at the synaptic level is not known. Here, we use in vivo patch-clamp recordings to show that locomotion can be directly read out from mossy fiber synaptic input and spike output in single granule cells. The increase in granule cell spiking during locomotion is enhanced by glutamate spillover currents recruited during movement. Surprisingly, the entire step sequence can be predicted from input EPSCs and output spikes of a single granule cell, suggesting that a robust gait code is present already at the cerebellar input layer and transmitted via the granule cell pathway to downstream Purkinje cells. Thus, synaptic input delivers remarkably rich information to single neurons during locomotion.

No MeSH data available.


Related in: MedlinePlus