Frequency response of vestibular reflexes in neck, back, and lower limb muscles

P.A. Forbes, C.J. Dakin, A.N. Vardy, R. Happee, G.P. Siegmund, Alfred Christiaan Schouten, J.S. Blouin

Research output: Contribution to journalArticleAcademicpeer-review

22 Citations (Scopus)

Abstract

Vestibular pathways form short-latency disynaptic connections with neck motoneurons, whereas they form longer-latency disynaptic and polysynaptic connections with lower limb motoneurons. We quantified frequency responses of vestibular reflexes in neck, back, and lower limb muscles to explain between-muscle differences. Two hypotheses were evaluated: 1) that muscle-specific motor-unit properties influence the bandwidth of vestibular reflexes; and 2) that frequency responses of vestibular reflexes differ between neck, back, and lower limb muscles because of neural filtering. Subjects were exposed to electrical vestibular stimuli over bandwidths of 0–25 and 0–75 Hz while recording activity in sternocleidomastoid, splenius capitis, erector spinae, soleus, and medial gastrocnemius muscles. Coherence between stimulus and muscle activity revealed markedly larger vestibular reflex bandwidths in neck muscles (0–70 Hz) than back (0–15 Hz) or lower limb muscles (0–20 Hz). In addition, vestibular reflexes in back and lower limb muscles undergo low-pass filtering compared with neck-muscle responses, which span a broader dynamic range. These results suggest that the wider bandwidth of head-neck biomechanics requires a vestibular influence on neck-muscle activation across a larger dynamic range than lower limb muscles. A computational model of vestibular afferents and a motoneuron pool indicates that motor-unit properties are not primary contributors to the bandwidth filtering of vestibular reflexes in different muscles. Instead, our experimental findings suggest that pathway-dependent neural filtering, not captured in our model, contributes to these muscle-specific responses. Furthermore, gain-phase discontinuities in the neck-muscle vestibular reflexes provide evidence of destructive interaction between different reflex components, likely via indirect vestibular-motor pathways
Original languageEnglish
Pages (from-to)1869-1881
Number of pages13
JournalJournal of neurophysiology
Volume110
Issue number8
DOIs
Publication statusPublished - 2013

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Reflex
Lower Extremity
Neck
Muscles
Neck Muscles
Motor Neurons
Paraspinal Muscles
Efferent Pathways
Neural Pathways
Biomechanical Phenomena
Skeletal Muscle
Head

Keywords

  • IR-90873
  • METIS-300435

Cite this

Forbes, P. A., Dakin, C. J., Vardy, A. N., Happee, R., Siegmund, G. P., Schouten, A. C., & Blouin, J. S. (2013). Frequency response of vestibular reflexes in neck, back, and lower limb muscles. Journal of neurophysiology, 110(8), 1869-1881. https://doi.org/10.1152/jn.00196.2013
Forbes, P.A. ; Dakin, C.J. ; Vardy, A.N. ; Happee, R. ; Siegmund, G.P. ; Schouten, Alfred Christiaan ; Blouin, J.S. / Frequency response of vestibular reflexes in neck, back, and lower limb muscles. In: Journal of neurophysiology. 2013 ; Vol. 110, No. 8. pp. 1869-1881.
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abstract = "Vestibular pathways form short-latency disynaptic connections with neck motoneurons, whereas they form longer-latency disynaptic and polysynaptic connections with lower limb motoneurons. We quantified frequency responses of vestibular reflexes in neck, back, and lower limb muscles to explain between-muscle differences. Two hypotheses were evaluated: 1) that muscle-specific motor-unit properties influence the bandwidth of vestibular reflexes; and 2) that frequency responses of vestibular reflexes differ between neck, back, and lower limb muscles because of neural filtering. Subjects were exposed to electrical vestibular stimuli over bandwidths of 0–25 and 0–75 Hz while recording activity in sternocleidomastoid, splenius capitis, erector spinae, soleus, and medial gastrocnemius muscles. Coherence between stimulus and muscle activity revealed markedly larger vestibular reflex bandwidths in neck muscles (0–70 Hz) than back (0–15 Hz) or lower limb muscles (0–20 Hz). In addition, vestibular reflexes in back and lower limb muscles undergo low-pass filtering compared with neck-muscle responses, which span a broader dynamic range. These results suggest that the wider bandwidth of head-neck biomechanics requires a vestibular influence on neck-muscle activation across a larger dynamic range than lower limb muscles. A computational model of vestibular afferents and a motoneuron pool indicates that motor-unit properties are not primary contributors to the bandwidth filtering of vestibular reflexes in different muscles. Instead, our experimental findings suggest that pathway-dependent neural filtering, not captured in our model, contributes to these muscle-specific responses. Furthermore, gain-phase discontinuities in the neck-muscle vestibular reflexes provide evidence of destructive interaction between different reflex components, likely via indirect vestibular-motor pathways",
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Forbes, PA, Dakin, CJ, Vardy, AN, Happee, R, Siegmund, GP, Schouten, AC & Blouin, JS 2013, 'Frequency response of vestibular reflexes in neck, back, and lower limb muscles' Journal of neurophysiology, vol. 110, no. 8, pp. 1869-1881. https://doi.org/10.1152/jn.00196.2013

Frequency response of vestibular reflexes in neck, back, and lower limb muscles. / Forbes, P.A.; Dakin, C.J.; Vardy, A.N.; Happee, R.; Siegmund, G.P.; Schouten, Alfred Christiaan; Blouin, J.S.

In: Journal of neurophysiology, Vol. 110, No. 8, 2013, p. 1869-1881.

Research output: Contribution to journalArticleAcademicpeer-review

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T1 - Frequency response of vestibular reflexes in neck, back, and lower limb muscles

AU - Forbes, P.A.

AU - Dakin, C.J.

AU - Vardy, A.N.

AU - Happee, R.

AU - Siegmund, G.P.

AU - Schouten, Alfred Christiaan

AU - Blouin, J.S.

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N2 - Vestibular pathways form short-latency disynaptic connections with neck motoneurons, whereas they form longer-latency disynaptic and polysynaptic connections with lower limb motoneurons. We quantified frequency responses of vestibular reflexes in neck, back, and lower limb muscles to explain between-muscle differences. Two hypotheses were evaluated: 1) that muscle-specific motor-unit properties influence the bandwidth of vestibular reflexes; and 2) that frequency responses of vestibular reflexes differ between neck, back, and lower limb muscles because of neural filtering. Subjects were exposed to electrical vestibular stimuli over bandwidths of 0–25 and 0–75 Hz while recording activity in sternocleidomastoid, splenius capitis, erector spinae, soleus, and medial gastrocnemius muscles. Coherence between stimulus and muscle activity revealed markedly larger vestibular reflex bandwidths in neck muscles (0–70 Hz) than back (0–15 Hz) or lower limb muscles (0–20 Hz). In addition, vestibular reflexes in back and lower limb muscles undergo low-pass filtering compared with neck-muscle responses, which span a broader dynamic range. These results suggest that the wider bandwidth of head-neck biomechanics requires a vestibular influence on neck-muscle activation across a larger dynamic range than lower limb muscles. A computational model of vestibular afferents and a motoneuron pool indicates that motor-unit properties are not primary contributors to the bandwidth filtering of vestibular reflexes in different muscles. Instead, our experimental findings suggest that pathway-dependent neural filtering, not captured in our model, contributes to these muscle-specific responses. Furthermore, gain-phase discontinuities in the neck-muscle vestibular reflexes provide evidence of destructive interaction between different reflex components, likely via indirect vestibular-motor pathways

AB - Vestibular pathways form short-latency disynaptic connections with neck motoneurons, whereas they form longer-latency disynaptic and polysynaptic connections with lower limb motoneurons. We quantified frequency responses of vestibular reflexes in neck, back, and lower limb muscles to explain between-muscle differences. Two hypotheses were evaluated: 1) that muscle-specific motor-unit properties influence the bandwidth of vestibular reflexes; and 2) that frequency responses of vestibular reflexes differ between neck, back, and lower limb muscles because of neural filtering. Subjects were exposed to electrical vestibular stimuli over bandwidths of 0–25 and 0–75 Hz while recording activity in sternocleidomastoid, splenius capitis, erector spinae, soleus, and medial gastrocnemius muscles. Coherence between stimulus and muscle activity revealed markedly larger vestibular reflex bandwidths in neck muscles (0–70 Hz) than back (0–15 Hz) or lower limb muscles (0–20 Hz). In addition, vestibular reflexes in back and lower limb muscles undergo low-pass filtering compared with neck-muscle responses, which span a broader dynamic range. These results suggest that the wider bandwidth of head-neck biomechanics requires a vestibular influence on neck-muscle activation across a larger dynamic range than lower limb muscles. A computational model of vestibular afferents and a motoneuron pool indicates that motor-unit properties are not primary contributors to the bandwidth filtering of vestibular reflexes in different muscles. Instead, our experimental findings suggest that pathway-dependent neural filtering, not captured in our model, contributes to these muscle-specific responses. Furthermore, gain-phase discontinuities in the neck-muscle vestibular reflexes provide evidence of destructive interaction between different reflex components, likely via indirect vestibular-motor pathways

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