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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

Tuning of responses to the step cycle.(A) Polar plot representing the step cycle modulation for each of the forelimb. Each of these plots is a representation of the step cycle for one recording (respectively an MFT, EPSC and GC spike recording), 0° being the start of the swing phase, the green line is end of the swing phase. Each trace (blue: left forelimb, red: right forelimb) represents as the radius in the plot the modulation of activity (see ‘Materials and methods’) for that phase of the step cycle (for the MFT plot, the scale corresponds to 2.4 Hz for the blue trace and 2.7 Hz for the red trace, for the EPSC plot the scale is 120 Hz for the blue trace and 65 Hz for the red trace, and for the GC spike trace, the scale is 13.6 Hz for the blue trace and 9.4 Hz for the red trace). The arrows show the phase of maximal modulation. Note that for these recordings, the maximal modulations are at roughly 90°. (B) The phases at which maximal modulation occurs can vary widely across cells for both the left and right forelimb (left and middle trace). The phase difference between these modulations for each cell is shown in the right panel. (C) The magnitude of modulation is highly correlated for the right and left limb across recording modalities (green: MFTS, red: EPSCs, blue: GC spikes). (D) The direction of maximum modulation is plotted here for all cells as a z-value (i.e., negative values indicate a decrease in activity and positive values an increase) for both the left and right forelimb.DOI:http://dx.doi.org/10.7554/eLife.07290.010
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fig4s2: Tuning of responses to the step cycle.(A) Polar plot representing the step cycle modulation for each of the forelimb. Each of these plots is a representation of the step cycle for one recording (respectively an MFT, EPSC and GC spike recording), 0° being the start of the swing phase, the green line is end of the swing phase. Each trace (blue: left forelimb, red: right forelimb) represents as the radius in the plot the modulation of activity (see ‘Materials and methods’) for that phase of the step cycle (for the MFT plot, the scale corresponds to 2.4 Hz for the blue trace and 2.7 Hz for the red trace, for the EPSC plot the scale is 120 Hz for the blue trace and 65 Hz for the red trace, and for the GC spike trace, the scale is 13.6 Hz for the blue trace and 9.4 Hz for the red trace). The arrows show the phase of maximal modulation. Note that for these recordings, the maximal modulations are at roughly 90°. (B) The phases at which maximal modulation occurs can vary widely across cells for both the left and right forelimb (left and middle trace). The phase difference between these modulations for each cell is shown in the right panel. (C) The magnitude of modulation is highly correlated for the right and left limb across recording modalities (green: MFTS, red: EPSCs, blue: GC spikes). (D) The direction of maximum modulation is plotted here for all cells as a z-value (i.e., negative values indicate a decrease in activity and positive values an increase) for both the left and right forelimb.DOI:http://dx.doi.org/10.7554/eLife.07290.010

Mentions: To examine in greater detail the tuning of events to the step cycle, we plotted the step cycle modulation of the event rates on a polar plot for both forelimbs. Mapping the start of the step cycle to 0° of the circle, we observed that cells could show maximal modulation in a wide range of phases (Figure 4—figure supplement 2; range from 0 to 351°). The phase difference between the maximal modulation for one forelimb vs the other was clustered around 90°: 102 ± 30° for MFTs, 104 ± 19.2 for EPSCs, 74 ± 15 for GC spikes. Not surprisingly, the magnitude of modulation was highly correlated between the two forelimbs (n = 20 cells, R = 0.9, p = 3.48 × 10−8). However as the MFT example in Figure 4A makes clear, not all modulations of activity were in the same direction for both forelimbs. In the right panel of Figure 4—figure supplement 2C, we have plotted the maximum modulations as z-scores for one limb vs the other, which shows across the population that modulations can happen in all four directions (up-up, up-down, down-up, down-down).


Synaptic representation of locomotion in single cerebellar granule cells.

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

Tuning of responses to the step cycle.(A) Polar plot representing the step cycle modulation for each of the forelimb. Each of these plots is a representation of the step cycle for one recording (respectively an MFT, EPSC and GC spike recording), 0° being the start of the swing phase, the green line is end of the swing phase. Each trace (blue: left forelimb, red: right forelimb) represents as the radius in the plot the modulation of activity (see ‘Materials and methods’) for that phase of the step cycle (for the MFT plot, the scale corresponds to 2.4 Hz for the blue trace and 2.7 Hz for the red trace, for the EPSC plot the scale is 120 Hz for the blue trace and 65 Hz for the red trace, and for the GC spike trace, the scale is 13.6 Hz for the blue trace and 9.4 Hz for the red trace). The arrows show the phase of maximal modulation. Note that for these recordings, the maximal modulations are at roughly 90°. (B) The phases at which maximal modulation occurs can vary widely across cells for both the left and right forelimb (left and middle trace). The phase difference between these modulations for each cell is shown in the right panel. (C) The magnitude of modulation is highly correlated for the right and left limb across recording modalities (green: MFTS, red: EPSCs, blue: GC spikes). (D) The direction of maximum modulation is plotted here for all cells as a z-value (i.e., negative values indicate a decrease in activity and positive values an increase) for both the left and right forelimb.DOI:http://dx.doi.org/10.7554/eLife.07290.010
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4499793&req=5

fig4s2: Tuning of responses to the step cycle.(A) Polar plot representing the step cycle modulation for each of the forelimb. Each of these plots is a representation of the step cycle for one recording (respectively an MFT, EPSC and GC spike recording), 0° being the start of the swing phase, the green line is end of the swing phase. Each trace (blue: left forelimb, red: right forelimb) represents as the radius in the plot the modulation of activity (see ‘Materials and methods’) for that phase of the step cycle (for the MFT plot, the scale corresponds to 2.4 Hz for the blue trace and 2.7 Hz for the red trace, for the EPSC plot the scale is 120 Hz for the blue trace and 65 Hz for the red trace, and for the GC spike trace, the scale is 13.6 Hz for the blue trace and 9.4 Hz for the red trace). The arrows show the phase of maximal modulation. Note that for these recordings, the maximal modulations are at roughly 90°. (B) The phases at which maximal modulation occurs can vary widely across cells for both the left and right forelimb (left and middle trace). The phase difference between these modulations for each cell is shown in the right panel. (C) The magnitude of modulation is highly correlated for the right and left limb across recording modalities (green: MFTS, red: EPSCs, blue: GC spikes). (D) The direction of maximum modulation is plotted here for all cells as a z-value (i.e., negative values indicate a decrease in activity and positive values an increase) for both the left and right forelimb.DOI:http://dx.doi.org/10.7554/eLife.07290.010
Mentions: To examine in greater detail the tuning of events to the step cycle, we plotted the step cycle modulation of the event rates on a polar plot for both forelimbs. Mapping the start of the step cycle to 0° of the circle, we observed that cells could show maximal modulation in a wide range of phases (Figure 4—figure supplement 2; range from 0 to 351°). The phase difference between the maximal modulation for one forelimb vs the other was clustered around 90°: 102 ± 30° for MFTs, 104 ± 19.2 for EPSCs, 74 ± 15 for GC spikes. Not surprisingly, the magnitude of modulation was highly correlated between the two forelimbs (n = 20 cells, R = 0.9, p = 3.48 × 10−8). However as the MFT example in Figure 4A makes clear, not all modulations of activity were in the same direction for both forelimbs. In the right panel of Figure 4—figure supplement 2C, we have plotted the maximum modulations as z-scores for one limb vs the other, which shows across the population that modulations can happen in all four directions (up-up, up-down, down-up, down-down).

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