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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

Attenuation of information association capability during motor learning. (A) A 5-s recording of the same PC SS activity with its fSS and ω during the third minute of balancing on the dowel (the corresponding data during the second minute being shown in Figure 4A). Signs of correlation between fSS and ω was not as apparent as in Figure 4A. (B) During periods with comparable movement levels ( = 30± 2.5°/s2) (a–f),  decreased suddenly (e.g., in period c). (C) The ratio of , but not r2, to the value in the first period decreased significantly during motor learning for many PCs (n = 10 of 17) (the same colored data in left and right part of (C) are from the same cell, but the color code bears no relationship to earlier plots). These results show the dynamic nature of the changes in the information association capability  during motor learning.
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Figure 7: Attenuation of information association capability during motor learning. (A) A 5-s recording of the same PC SS activity with its fSS and ω during the third minute of balancing on the dowel (the corresponding data during the second minute being shown in Figure 4A). Signs of correlation between fSS and ω was not as apparent as in Figure 4A. (B) During periods with comparable movement levels ( = 30± 2.5°/s2) (a–f), decreased suddenly (e.g., in period c). (C) The ratio of , but not r2, to the value in the first period decreased significantly during motor learning for many PCs (n = 10 of 17) (the same colored data in left and right part of (C) are from the same cell, but the color code bears no relationship to earlier plots). These results show the dynamic nature of the changes in the information association capability during motor learning.

Mentions: A critical test in the present study was to determine how SS coding of sensory information was modulated as the rats learned to balance on the dowel. Figure 7A shows a typical PC in which the correlation between SS firing and head movement in the third minute on the dowel appeared to be weaker than that in the second minute (Figure 4A, same PC). Changes such as those shown in Figures 4A, 7A were routinely observed in the PCs of the present study. also seemed to become more variable with training while decreased (Figure 6B). However, since and r2 correlated positively with (Figure 6) and decreased during the time on the dowel (Figure 1), the decrease of during balancing may simply be due to the decrease in . To reduce the influence of on the association between SS firing and head-body movement, periods with comparable were selected to test the attenuation of their association (Methods; Figures 7Ba–f). r2 fluctuated through the periods with comparable , however, a sudden drop of occurred during the period on the dowel (Figure 7B, right panel). For the 17 PCs with SSs encoding θ or ω, 10 ω-coding cells became unresponsive with over 50% attenuation in (23.42 ± 0.02%; intercepted s were ranged from 20 to 70°/s2; Figure 7C).


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)

Attenuation of information association capability during motor learning. (A) A 5-s recording of the same PC SS activity with its fSS and ω during the third minute of balancing on the dowel (the corresponding data during the second minute being shown in Figure 4A). Signs of correlation between fSS and ω was not as apparent as in Figure 4A. (B) During periods with comparable movement levels ( = 30± 2.5°/s2) (a–f),  decreased suddenly (e.g., in period c). (C) The ratio of , but not r2, to the value in the first period decreased significantly during motor learning for many PCs (n = 10 of 17) (the same colored data in left and right part of (C) are from the same cell, but the color code bears no relationship to earlier plots). These results show the dynamic nature of the changes in the information association capability  during motor learning.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4524947&req=5

Figure 7: Attenuation of information association capability during motor learning. (A) A 5-s recording of the same PC SS activity with its fSS and ω during the third minute of balancing on the dowel (the corresponding data during the second minute being shown in Figure 4A). Signs of correlation between fSS and ω was not as apparent as in Figure 4A. (B) During periods with comparable movement levels ( = 30± 2.5°/s2) (a–f), decreased suddenly (e.g., in period c). (C) The ratio of , but not r2, to the value in the first period decreased significantly during motor learning for many PCs (n = 10 of 17) (the same colored data in left and right part of (C) are from the same cell, but the color code bears no relationship to earlier plots). These results show the dynamic nature of the changes in the information association capability during motor learning.
Mentions: A critical test in the present study was to determine how SS coding of sensory information was modulated as the rats learned to balance on the dowel. Figure 7A shows a typical PC in which the correlation between SS firing and head movement in the third minute on the dowel appeared to be weaker than that in the second minute (Figure 4A, same PC). Changes such as those shown in Figures 4A, 7A were routinely observed in the PCs of the present study. also seemed to become more variable with training while decreased (Figure 6B). However, since and r2 correlated positively with (Figure 6) and decreased during the time on the dowel (Figure 1), the decrease of during balancing may simply be due to the decrease in . To reduce the influence of on the association between SS firing and head-body movement, periods with comparable were selected to test the attenuation of their association (Methods; Figures 7Ba–f). r2 fluctuated through the periods with comparable , however, a sudden drop of occurred during the period on the dowel (Figure 7B, right panel). For the 17 PCs with SSs encoding θ or ω, 10 ω-coding cells became unresponsive with over 50% attenuation in (23.42 ± 0.02%; intercepted s were ranged from 20 to 70°/s2; Figure 7C).

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