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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

Whole-cell recordings from granule cells and mossy fibers during locomotion.(A) Schematic of recording configuration. (B) Calculation of motion index. Top panel: a single frame from a video of a mouse walking on the treadmill. Bottom panel: pixel intensity variation between the frame shown in the above panel and the previous frame are highlighted in red. The pixel variation between each frame was quantified for each video to give a continuous signal relating to average motion of the mouse (motion index calculated as described in the ‘Materials and methods’ and normalized to the maximum value in the video). (C–E) Example whole-cell recordings (black) from a presynaptic mossy fiber terminal (C), a granule cell recorded in voltage-clamp mode (D) and a granule cell recorded in current clamp mode (E), together with the corresponding motion index (red). (F–H) Section of each example trace shown in C–E at a higher timescale show spontaneous input recorded during a quiet period (left panels, orange frames in (C–E) indicate the location within the trace) and typical bursts of activity during locomotion (right panels, blue frames in (C–E) indicate the location within the trace). Summary data comparing the average instantaneous frequencies of mossy fiber spikes (I, n = 4 in 4 mice), granule cell EPSCs (J, n = 9 in 6 mice) and granule cell spikes (K, n = 6, in 4 mice). Mean group averages are indicated with black open and closed circles, error bars indicate standard deviation.DOI:http://dx.doi.org/10.7554/eLife.07290.003
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fig1: Whole-cell recordings from granule cells and mossy fibers during locomotion.(A) Schematic of recording configuration. (B) Calculation of motion index. Top panel: a single frame from a video of a mouse walking on the treadmill. Bottom panel: pixel intensity variation between the frame shown in the above panel and the previous frame are highlighted in red. The pixel variation between each frame was quantified for each video to give a continuous signal relating to average motion of the mouse (motion index calculated as described in the ‘Materials and methods’ and normalized to the maximum value in the video). (C–E) Example whole-cell recordings (black) from a presynaptic mossy fiber terminal (C), a granule cell recorded in voltage-clamp mode (D) and a granule cell recorded in current clamp mode (E), together with the corresponding motion index (red). (F–H) Section of each example trace shown in C–E at a higher timescale show spontaneous input recorded during a quiet period (left panels, orange frames in (C–E) indicate the location within the trace) and typical bursts of activity during locomotion (right panels, blue frames in (C–E) indicate the location within the trace). Summary data comparing the average instantaneous frequencies of mossy fiber spikes (I, n = 4 in 4 mice), granule cell EPSCs (J, n = 9 in 6 mice) and granule cell spikes (K, n = 6, in 4 mice). Mean group averages are indicated with black open and closed circles, error bars indicate standard deviation.DOI:http://dx.doi.org/10.7554/eLife.07290.003

Mentions: In vivo whole-cell recordings were made from mossy fiber boutons and cerebellar granule cells in lobule V of the cerebellar vermis. All recordings were performed in awake mice head-fixed on a spherical treadmill (Figure 1A). Granule cells and mossy fiber boutons were identified on the basis of their distinctive electrophysiological signatures (Chadderton et al., 2004; Jörntell and Ekerot, 2006; Rancz et al., 2007; Arenz et al., 2008). To study the link between voluntary movement and granule cell input and output we extracted a motion index from captured video frames (Figure 1B, see ‘Materials and methods’) and aligned this to the simultaneously acquired electrophysiological data (example recordings Figure 1C–E). The motion index was used to categorize the electrophysiological data recorded during quiet wakefulness (defined as periods where the motion index remained below a threshold rate of change of 0.025 a.u. per frame, for at least 30 consecutive frames, see ‘Materials and methods’) and voluntary movement.10.7554/eLife.07290.003Figure 1.Whole-cell recordings from granule cells and mossy fibers during locomotion.


Synaptic representation of locomotion in single cerebellar granule cells.

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

Whole-cell recordings from granule cells and mossy fibers during locomotion.(A) Schematic of recording configuration. (B) Calculation of motion index. Top panel: a single frame from a video of a mouse walking on the treadmill. Bottom panel: pixel intensity variation between the frame shown in the above panel and the previous frame are highlighted in red. The pixel variation between each frame was quantified for each video to give a continuous signal relating to average motion of the mouse (motion index calculated as described in the ‘Materials and methods’ and normalized to the maximum value in the video). (C–E) Example whole-cell recordings (black) from a presynaptic mossy fiber terminal (C), a granule cell recorded in voltage-clamp mode (D) and a granule cell recorded in current clamp mode (E), together with the corresponding motion index (red). (F–H) Section of each example trace shown in C–E at a higher timescale show spontaneous input recorded during a quiet period (left panels, orange frames in (C–E) indicate the location within the trace) and typical bursts of activity during locomotion (right panels, blue frames in (C–E) indicate the location within the trace). Summary data comparing the average instantaneous frequencies of mossy fiber spikes (I, n = 4 in 4 mice), granule cell EPSCs (J, n = 9 in 6 mice) and granule cell spikes (K, n = 6, in 4 mice). Mean group averages are indicated with black open and closed circles, error bars indicate standard deviation.DOI:http://dx.doi.org/10.7554/eLife.07290.003
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fig1: Whole-cell recordings from granule cells and mossy fibers during locomotion.(A) Schematic of recording configuration. (B) Calculation of motion index. Top panel: a single frame from a video of a mouse walking on the treadmill. Bottom panel: pixel intensity variation between the frame shown in the above panel and the previous frame are highlighted in red. The pixel variation between each frame was quantified for each video to give a continuous signal relating to average motion of the mouse (motion index calculated as described in the ‘Materials and methods’ and normalized to the maximum value in the video). (C–E) Example whole-cell recordings (black) from a presynaptic mossy fiber terminal (C), a granule cell recorded in voltage-clamp mode (D) and a granule cell recorded in current clamp mode (E), together with the corresponding motion index (red). (F–H) Section of each example trace shown in C–E at a higher timescale show spontaneous input recorded during a quiet period (left panels, orange frames in (C–E) indicate the location within the trace) and typical bursts of activity during locomotion (right panels, blue frames in (C–E) indicate the location within the trace). Summary data comparing the average instantaneous frequencies of mossy fiber spikes (I, n = 4 in 4 mice), granule cell EPSCs (J, n = 9 in 6 mice) and granule cell spikes (K, n = 6, in 4 mice). Mean group averages are indicated with black open and closed circles, error bars indicate standard deviation.DOI:http://dx.doi.org/10.7554/eLife.07290.003
Mentions: In vivo whole-cell recordings were made from mossy fiber boutons and cerebellar granule cells in lobule V of the cerebellar vermis. All recordings were performed in awake mice head-fixed on a spherical treadmill (Figure 1A). Granule cells and mossy fiber boutons were identified on the basis of their distinctive electrophysiological signatures (Chadderton et al., 2004; Jörntell and Ekerot, 2006; Rancz et al., 2007; Arenz et al., 2008). To study the link between voluntary movement and granule cell input and output we extracted a motion index from captured video frames (Figure 1B, see ‘Materials and methods’) and aligned this to the simultaneously acquired electrophysiological data (example recordings Figure 1C–E). The motion index was used to categorize the electrophysiological data recorded during quiet wakefulness (defined as periods where the motion index remained below a threshold rate of change of 0.025 a.u. per frame, for at least 30 consecutive frames, see ‘Materials and methods’) and voluntary movement.10.7554/eLife.07290.003Figure 1.Whole-cell recordings from granule cells and mossy fibers during locomotion.

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