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Functional changes in muscle afferent neurones in an osteoarthritis model: implications for impaired proprioceptive performance.

Wu Q, Henry JL - PLoS ONE (2012)

Bottom Line: Depolarizing intracellular current injection elicited more APs in models than in naïve muscle afferent neurones (P = 0.01) indicating greater excitability.The present study demonstrates changes in hind limb stance accompanied by changes in the functional properties of muscle afferent neurones in this derangement model of OA.This may provide a possible avenue to explore mechanisms underlying the impaired proprioceptive performance and perhaps other sensory disorders in people with OA.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychiatry and Behavioural Neurosciences, McMaster University, Hamilton, Ontario, Canada.

ABSTRACT

Background: Impaired proprioceptive performance is a significant clinical issue for many who suffer osteoarthritis (OA) and is a risk factor for falls and other liabilities. This study was designed to evaluate weight-bearing distribution in a rat model of OA and to determine whether changes also occur in muscle afferent neurones.

Methodology/principal findings: Intracellular recordings were made in functionally identified dorsal root ganglion neurones in acute electrophysiological experiments on the anaesthetized animal following measurements of hind limb weight bearing in the incapacitance test. OA rats but not naïve control rats stood with less weight on the ipsilateral hind leg (P = 0.02). In the acute electrophysiological experiments that followed weight bearing measurements, action potentials (AP) elicited by electrical stimulation of the dorsal roots differed in OA rats, including longer AP duration (P = 0.006), slower rise time (P = 0.001) and slower maximum rising rate (P = 0.03). Depolarizing intracellular current injection elicited more APs in models than in naïve muscle afferent neurones (P = 0.01) indicating greater excitability. Axonal conduction velocity in model animals was slower (P = 0.04).

Conclusions/significance: The present study demonstrates changes in hind limb stance accompanied by changes in the functional properties of muscle afferent neurones in this derangement model of OA. This may provide a possible avenue to explore mechanisms underlying the impaired proprioceptive performance and perhaps other sensory disorders in people with OA.

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Excitability of muscle afferent neurones determined by depolarizing current injection in control and OA animals.2nA direct current was injected into neurones at 4 weeks after surgery in control and in OA animals. (A and B) show repetitive firing in a control and an OA muscle afferent neurone, respectively. In both recordings, the upper trace indicates the 2 nA depolarizing current, and the lower trace is the intracellular recording signal. (C) Shows the histogram showing the number of neurones with various evoked APs following depolarizing current injection in both control and OA muscle afferent neurones. (D) Shows the comparison of the number of APs evoked by 2 nA direct current injection between OA (N = 37) and control (N = 25) muscle afferent neurones. The Mann-Whitney U-test was used.
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pone-0036854-g005: Excitability of muscle afferent neurones determined by depolarizing current injection in control and OA animals.2nA direct current was injected into neurones at 4 weeks after surgery in control and in OA animals. (A and B) show repetitive firing in a control and an OA muscle afferent neurone, respectively. In both recordings, the upper trace indicates the 2 nA depolarizing current, and the lower trace is the intracellular recording signal. (C) Shows the histogram showing the number of neurones with various evoked APs following depolarizing current injection in both control and OA muscle afferent neurones. (D) Shows the comparison of the number of APs evoked by 2 nA direct current injection between OA (N = 37) and control (N = 25) muscle afferent neurones. The Mann-Whitney U-test was used.

Mentions: Somata excitability was determined by direct depolarizing current injection into the neurone via the recording pipette. Examples of repetitive firing during direct current injection from muscle afferent neurones in control and OA model animals are shown in Figure 5A, 5B; there was a greater percentage of neurones exhibiting seven or more APs in OA animals: 45.9% in OA (N = 25) vs. 16.1% in control (N = 37). In addition, 68% of control muscle afferent neurones exhibited only one AP (36.1%) or no AP (32.2%) following a 20 ms, 2nA depolarizing current injection. In neurones from OA animals this percentage was considerably less, at 32.4%: one AP (18.9%), no AP (13.5%). These differences indicate a significant shift towards greater repetitive firing frequencies during current injection in OA animals (Chi-square test, P = 0.02). A detailed composition of APs in both groups of neurone is shown in Figure 5C. The average number of APs following the 20 ms, 2nA depolarizing current injection was 2.28±0.59 (N = 25) in the control muscle afferent neurones. This number was greater in OA muscle afferent neurones, at 4.73±0.57 (N = 37; Mann-Whitney U-test, P = 0.01; Figure 5D), indicating a greater neuronal excitability in muscle afferent neurones in OA animals.


Functional changes in muscle afferent neurones in an osteoarthritis model: implications for impaired proprioceptive performance.

Wu Q, Henry JL - PLoS ONE (2012)

Excitability of muscle afferent neurones determined by depolarizing current injection in control and OA animals.2nA direct current was injected into neurones at 4 weeks after surgery in control and in OA animals. (A and B) show repetitive firing in a control and an OA muscle afferent neurone, respectively. In both recordings, the upper trace indicates the 2 nA depolarizing current, and the lower trace is the intracellular recording signal. (C) Shows the histogram showing the number of neurones with various evoked APs following depolarizing current injection in both control and OA muscle afferent neurones. (D) Shows the comparison of the number of APs evoked by 2 nA direct current injection between OA (N = 37) and control (N = 25) muscle afferent neurones. The Mann-Whitney U-test was used.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3351471&req=5

pone-0036854-g005: Excitability of muscle afferent neurones determined by depolarizing current injection in control and OA animals.2nA direct current was injected into neurones at 4 weeks after surgery in control and in OA animals. (A and B) show repetitive firing in a control and an OA muscle afferent neurone, respectively. In both recordings, the upper trace indicates the 2 nA depolarizing current, and the lower trace is the intracellular recording signal. (C) Shows the histogram showing the number of neurones with various evoked APs following depolarizing current injection in both control and OA muscle afferent neurones. (D) Shows the comparison of the number of APs evoked by 2 nA direct current injection between OA (N = 37) and control (N = 25) muscle afferent neurones. The Mann-Whitney U-test was used.
Mentions: Somata excitability was determined by direct depolarizing current injection into the neurone via the recording pipette. Examples of repetitive firing during direct current injection from muscle afferent neurones in control and OA model animals are shown in Figure 5A, 5B; there was a greater percentage of neurones exhibiting seven or more APs in OA animals: 45.9% in OA (N = 25) vs. 16.1% in control (N = 37). In addition, 68% of control muscle afferent neurones exhibited only one AP (36.1%) or no AP (32.2%) following a 20 ms, 2nA depolarizing current injection. In neurones from OA animals this percentage was considerably less, at 32.4%: one AP (18.9%), no AP (13.5%). These differences indicate a significant shift towards greater repetitive firing frequencies during current injection in OA animals (Chi-square test, P = 0.02). A detailed composition of APs in both groups of neurone is shown in Figure 5C. The average number of APs following the 20 ms, 2nA depolarizing current injection was 2.28±0.59 (N = 25) in the control muscle afferent neurones. This number was greater in OA muscle afferent neurones, at 4.73±0.57 (N = 37; Mann-Whitney U-test, P = 0.01; Figure 5D), indicating a greater neuronal excitability in muscle afferent neurones in OA animals.

Bottom Line: Depolarizing intracellular current injection elicited more APs in models than in naïve muscle afferent neurones (P = 0.01) indicating greater excitability.The present study demonstrates changes in hind limb stance accompanied by changes in the functional properties of muscle afferent neurones in this derangement model of OA.This may provide a possible avenue to explore mechanisms underlying the impaired proprioceptive performance and perhaps other sensory disorders in people with OA.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychiatry and Behavioural Neurosciences, McMaster University, Hamilton, Ontario, Canada.

ABSTRACT

Background: Impaired proprioceptive performance is a significant clinical issue for many who suffer osteoarthritis (OA) and is a risk factor for falls and other liabilities. This study was designed to evaluate weight-bearing distribution in a rat model of OA and to determine whether changes also occur in muscle afferent neurones.

Methodology/principal findings: Intracellular recordings were made in functionally identified dorsal root ganglion neurones in acute electrophysiological experiments on the anaesthetized animal following measurements of hind limb weight bearing in the incapacitance test. OA rats but not naïve control rats stood with less weight on the ipsilateral hind leg (P = 0.02). In the acute electrophysiological experiments that followed weight bearing measurements, action potentials (AP) elicited by electrical stimulation of the dorsal roots differed in OA rats, including longer AP duration (P = 0.006), slower rise time (P = 0.001) and slower maximum rising rate (P = 0.03). Depolarizing intracellular current injection elicited more APs in models than in naïve muscle afferent neurones (P = 0.01) indicating greater excitability. Axonal conduction velocity in model animals was slower (P = 0.04).

Conclusions/significance: The present study demonstrates changes in hind limb stance accompanied by changes in the functional properties of muscle afferent neurones in this derangement model of OA. This may provide a possible avenue to explore mechanisms underlying the impaired proprioceptive performance and perhaps other sensory disorders in people with OA.

Show MeSH
Related in: MedlinePlus