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Plasticity of cerebellar Purkinje cells in behavioral training of body balance control.

Lee RX, Huang JJ, Huang C, Tsai ML, Yen CT - Front Syst Neurosci (2015)

Bottom Line: The ability to differentiate such sensory information can lead to movement execution with better accuracy.Both PC simple (SSs; 17 of 26) and complex spikes (CSs; 7 of 12) were found to code initially on the angle of the heads with respect to a fixed reference.Using periods with comparable degrees of movement, we found that such SS coding of information in most PCs (10 of 17) decreased rapidly during balance learning.

View Article: PubMed Central - PubMed

Affiliation: Department of Life Science, National Taiwan University Taipei, Taiwan.

ABSTRACT
Neural responses to sensory inputs caused by self-generated movements (reafference) and external passive stimulation (exafference) differ in various brain regions. The ability to differentiate such sensory information can lead to movement execution with better accuracy. However, how sensory responses are adjusted in regard to this distinguishability during motor learning is still poorly understood. The cerebellum has been hypothesized to analyze the functional significance of sensory information during motor learning, and is thought to be a key region of reafference computation in the vestibular system. In this study, we investigated Purkinje cell (PC) spike trains as cerebellar cortical output when rats learned to balance on a suspended dowel. Rats progressively reduced the amplitude of body swing and made fewer foot slips during a 5-min balancing task. Both PC simple (SSs; 17 of 26) and complex spikes (CSs; 7 of 12) were found to code initially on the angle of the heads with respect to a fixed reference. Using periods with comparable degrees of movement, we found that such SS coding of information in most PCs (10 of 17) decreased rapidly during balance learning. In response to unexpected perturbations and under anesthesia, SS coding capability of these PCs recovered. By plotting SS and CS firing frequencies over 15-s time windows in double-logarithmic plots, a negative correlation between SS and CS was found in awake, but not anesthetized, rats. PCs with prominent SS coding attenuation during motor learning showed weaker SS-CS correlation. Hence, we demonstrate that neural plasticity for filtering out sensory reafference from active motion occurs in the cerebellar cortex in rats during balance learning. SS-CS interaction may contribute to this rapid plasticity as a form of receptive field plasticity in the cerebellar cortex between two receptive maps of sensory inputs from the external world and of efference copies from the will center for volitional movements.

No MeSH data available.


Related in: MedlinePlus

Coding capability remained the same during passive stimulation. Simple traces of the same PC (as in Figures 4A, 7A) showed coding of ω during (A) additional perturbations (green dashed line shows the starting point of the perturbation) and (B) stimulation under anesthesia. (C) showed no time-dependent change due to passive perturbation (upper panel) or by a sustained vestibular stimulus under anesthesia (low panel). (D) tested under different behavioral and physiological states. First, the first analyzed period on the dowel; Last, the last analyzed period on the dowel; Pert.—On dowel, unexpected perturbation when a rat was on the dowel; Pert.—Anesthetized, perturbation when a rat was under anesthesia.
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Figure 9: Coding capability remained the same during passive stimulation. Simple traces of the same PC (as in Figures 4A, 7A) showed coding of ω during (A) additional perturbations (green dashed line shows the starting point of the perturbation) and (B) stimulation under anesthesia. (C) showed no time-dependent change due to passive perturbation (upper panel) or by a sustained vestibular stimulus under anesthesia (low panel). (D) tested under different behavioral and physiological states. First, the first analyzed period on the dowel; Last, the last analyzed period on the dowel; Pert.—On dowel, unexpected perturbation when a rat was on the dowel; Pert.—Anesthetized, perturbation when a rat was under anesthesia.

Mentions: To inquire whether attenuation in SS information coding observed in Figure 7 was indeed related to motor learning, we introduced additional perturbations at irregular time intervals by transiently shaking the balance apparatus after the 5-min recording of the balancing behavior. SS firing responded to head movement during these additional perturbations (Figure 9A), with value of similar to that before response attenuation (1.11 ± 0.27 Hz/(°/s) before attenuation vs. 1.344 ± 0.21 Hz/(°/s) after the additional perturbations, p = 0.407, Student's t-test; Figure 9D). In addition, sensory responses of SS still encoded head motion under anesthesia (Figure 9B), with maintained at a level higher than that before response attenuation (2.88 ± 0.60 Hz/(°/s); p = 0.028, Student's t-test; Figures 9C,D). These results suggest that SS information coding attenuation during motor learning may be a selective filtering of reafference information.


Plasticity of cerebellar Purkinje cells in behavioral training of body balance control.

Lee RX, Huang JJ, Huang C, Tsai ML, Yen CT - Front Syst Neurosci (2015)

Coding capability remained the same during passive stimulation. Simple traces of the same PC (as in Figures 4A, 7A) showed coding of ω during (A) additional perturbations (green dashed line shows the starting point of the perturbation) and (B) stimulation under anesthesia. (C) showed no time-dependent change due to passive perturbation (upper panel) or by a sustained vestibular stimulus under anesthesia (low panel). (D) tested under different behavioral and physiological states. First, the first analyzed period on the dowel; Last, the last analyzed period on the dowel; Pert.—On dowel, unexpected perturbation when a rat was on the dowel; Pert.—Anesthetized, perturbation when a rat was under anesthesia.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4524947&req=5

Figure 9: Coding capability remained the same during passive stimulation. Simple traces of the same PC (as in Figures 4A, 7A) showed coding of ω during (A) additional perturbations (green dashed line shows the starting point of the perturbation) and (B) stimulation under anesthesia. (C) showed no time-dependent change due to passive perturbation (upper panel) or by a sustained vestibular stimulus under anesthesia (low panel). (D) tested under different behavioral and physiological states. First, the first analyzed period on the dowel; Last, the last analyzed period on the dowel; Pert.—On dowel, unexpected perturbation when a rat was on the dowel; Pert.—Anesthetized, perturbation when a rat was under anesthesia.
Mentions: To inquire whether attenuation in SS information coding observed in Figure 7 was indeed related to motor learning, we introduced additional perturbations at irregular time intervals by transiently shaking the balance apparatus after the 5-min recording of the balancing behavior. SS firing responded to head movement during these additional perturbations (Figure 9A), with value of similar to that before response attenuation (1.11 ± 0.27 Hz/(°/s) before attenuation vs. 1.344 ± 0.21 Hz/(°/s) after the additional perturbations, p = 0.407, Student's t-test; Figure 9D). In addition, sensory responses of SS still encoded head motion under anesthesia (Figure 9B), with maintained at a level higher than that before response attenuation (2.88 ± 0.60 Hz/(°/s); p = 0.028, Student's t-test; Figures 9C,D). These results suggest that SS information coding attenuation during motor learning may be a selective filtering of reafference information.

Bottom Line: The ability to differentiate such sensory information can lead to movement execution with better accuracy.Both PC simple (SSs; 17 of 26) and complex spikes (CSs; 7 of 12) were found to code initially on the angle of the heads with respect to a fixed reference.Using periods with comparable degrees of movement, we found that such SS coding of information in most PCs (10 of 17) decreased rapidly during balance learning.

View Article: PubMed Central - PubMed

Affiliation: Department of Life Science, National Taiwan University Taipei, Taiwan.

ABSTRACT
Neural responses to sensory inputs caused by self-generated movements (reafference) and external passive stimulation (exafference) differ in various brain regions. The ability to differentiate such sensory information can lead to movement execution with better accuracy. However, how sensory responses are adjusted in regard to this distinguishability during motor learning is still poorly understood. The cerebellum has been hypothesized to analyze the functional significance of sensory information during motor learning, and is thought to be a key region of reafference computation in the vestibular system. In this study, we investigated Purkinje cell (PC) spike trains as cerebellar cortical output when rats learned to balance on a suspended dowel. Rats progressively reduced the amplitude of body swing and made fewer foot slips during a 5-min balancing task. Both PC simple (SSs; 17 of 26) and complex spikes (CSs; 7 of 12) were found to code initially on the angle of the heads with respect to a fixed reference. Using periods with comparable degrees of movement, we found that such SS coding of information in most PCs (10 of 17) decreased rapidly during balance learning. In response to unexpected perturbations and under anesthesia, SS coding capability of these PCs recovered. By plotting SS and CS firing frequencies over 15-s time windows in double-logarithmic plots, a negative correlation between SS and CS was found in awake, but not anesthetized, rats. PCs with prominent SS coding attenuation during motor learning showed weaker SS-CS correlation. Hence, we demonstrate that neural plasticity for filtering out sensory reafference from active motion occurs in the cerebellar cortex in rats during balance learning. SS-CS interaction may contribute to this rapid plasticity as a form of receptive field plasticity in the cerebellar cortex between two receptive maps of sensory inputs from the external world and of efference copies from the will center for volitional movements.

No MeSH data available.


Related in: MedlinePlus