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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 attenuation was not related to less dowel movement. (A) To quantify the magnitude of dowel perturbation [; defined by the equation shown in (A)], we recoded the swing angle of dowel perturbation ϕ and defined  as the sum of the absolute values of the ϕ changing rate (ωϕ) in a period divided by the length of time. (B) did not differ significantly before and after attenuation in  occurred (periods with comparable movement levels above and below 50% attenuation; p = 0.566, Student's t-test). This result suggests that coding capability attenuation was not related to a reduction in dowel movement.
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Figure 8: Coding capability attenuation was not related to less dowel movement. (A) To quantify the magnitude of dowel perturbation [; defined by the equation shown in (A)], we recoded the swing angle of dowel perturbation ϕ and defined as the sum of the absolute values of the ϕ changing rate (ωϕ) in a period divided by the length of time. (B) did not differ significantly before and after attenuation in occurred (periods with comparable movement levels above and below 50% attenuation; p = 0.566, Student's t-test). This result suggests that coding capability attenuation was not related to a reduction in dowel movement.

Mentions: In the rostral fastigial neurons of monkeys, active movement was accompanied by weaker sensory responses than passive movements (Brooks and Cullen, 2013). Despite the prevailing view that CS discharge responds to passive motion caused by error events (Ito, 1972), some investigators thought that SS discharges encode errors (Popa et al., 2012, 2013). Perhaps attenuation in in these PCs is caused by decreasing passive movement during the motor learning as a response to state transformation in the weight between active and passive movement. To distinguish directly between active and passive movement in freely behaving animals is challenging; however, we tried to indirectly distinguish components of active and passive motion from video recordings during balancing. When rats moved voluntarily on the dowel, the passive motion component may be represented in perturbations of the hanging dowel. To quantify perturbation of the dowel (), which might be positively correlated with the level of passive motion, we recoded the swing amplitude of dowel perturbation (Figure 8A) and defined as the sum of the absolute values of the ϕ changing rate during a period divided by the length of the period. was not significantly different before and after attenuations occurred (p = 0.566, Student's t-test; Figure 8B), indicating that passive motion due to dowel swing was of similar magnitude during these periods. Thus, we demonstrate that attenuation in the of PCs is a result of the plasticity in PC responses to sensory 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 attenuation was not related to less dowel movement. (A) To quantify the magnitude of dowel perturbation [; defined by the equation shown in (A)], we recoded the swing angle of dowel perturbation ϕ and defined  as the sum of the absolute values of the ϕ changing rate (ωϕ) in a period divided by the length of time. (B) did not differ significantly before and after attenuation in  occurred (periods with comparable movement levels above and below 50% attenuation; p = 0.566, Student's t-test). This result suggests that coding capability attenuation was not related to a reduction in dowel movement.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 8: Coding capability attenuation was not related to less dowel movement. (A) To quantify the magnitude of dowel perturbation [; defined by the equation shown in (A)], we recoded the swing angle of dowel perturbation ϕ and defined as the sum of the absolute values of the ϕ changing rate (ωϕ) in a period divided by the length of time. (B) did not differ significantly before and after attenuation in occurred (periods with comparable movement levels above and below 50% attenuation; p = 0.566, Student's t-test). This result suggests that coding capability attenuation was not related to a reduction in dowel movement.
Mentions: In the rostral fastigial neurons of monkeys, active movement was accompanied by weaker sensory responses than passive movements (Brooks and Cullen, 2013). Despite the prevailing view that CS discharge responds to passive motion caused by error events (Ito, 1972), some investigators thought that SS discharges encode errors (Popa et al., 2012, 2013). Perhaps attenuation in in these PCs is caused by decreasing passive movement during the motor learning as a response to state transformation in the weight between active and passive movement. To distinguish directly between active and passive movement in freely behaving animals is challenging; however, we tried to indirectly distinguish components of active and passive motion from video recordings during balancing. When rats moved voluntarily on the dowel, the passive motion component may be represented in perturbations of the hanging dowel. To quantify perturbation of the dowel (), which might be positively correlated with the level of passive motion, we recoded the swing amplitude of dowel perturbation (Figure 8A) and defined as the sum of the absolute values of the ϕ changing rate during a period divided by the length of the period. was not significantly different before and after attenuations occurred (p = 0.566, Student's t-test; Figure 8B), indicating that passive motion due to dowel swing was of similar magnitude during these periods. Thus, we demonstrate that attenuation in the of PCs is a result of the plasticity in PC responses to sensory 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