Abstract
In sitting humans a rapid unexpected lengthening of the knee extensors elicits a stretch reflex (SR) response as recorded by the electromyogram (EMG) which comprises multiple bursts. These are termed short latency responses (SLR), medium latency responses (MLR) and long latency responses (LLR). The aim of this study was to determine if a transcortical pathway contributes to any of these bursts. Flexion perturbations (amplitude =4°, velocity=150°/s) were imposed on the right knee joint of sitting subjects (n=11). The effect of the perturbation on the electromyographic (EMG) response of the pre-contracted quadriceps muscle to magnetic stimulation of the contralateral motor cortex was quantified. Transcranial magnetic stimulation (TMS) was applied to elicit a compound motor evoked potential (MEP) in the target muscle rectus femoris (RF), in the vastus lateralis (VL), vastus medialis (VM) and biceps femoris (BF). The MEP and SR were elicited either in combination or separately. When applied in combination the delay between the SR and the MEP varied from 0 to 150 ms in steps of 4, 5 and 10 ms. Somatosensory evoked potentials (SEPs) were recorded from four subjects during the imposed stretch to quantify the latency of the resulting afferent volley. Onset latencies of responses in RF were 25±2 ms for the SR and 20±4 ms for the MEP. The average SEP latency was 24±2 ms. A transcortical pathway thus has the potential to contribute to the RF SR no earlier than 54±6 ms (SEP + MEP + 10 ms central processing delay) following the stretch onset. The duration of the total reflex burst was 85±6 ms. Significant facilitation of the MEP commenced at 78 ms, coinciding with the LLR component of the stretch response. No such facilitation was observed in the synergists VL and VM, or in the antagonist BF. Our results indicate that the LLR of the RF likely involves supraspinal pathways. More importantly, of the investigated muscles, this involvement of higher centers in the shaping of the LLR is specific to the RF muscle during the investigated task.
Similar content being viewed by others
References
Allum JH, Mauritz KH (1984) Compensation for intrinsic muscle stiffness by short-latency reflexes in human triceps surae muscles. J Neurophysiol 52:797–818
Allum JH, Mauritz KH, Vogele H (1982) Stiffness regulation provided by short-latency reflexes in human triceps surae muscles. Brain Res 234:159–164
Bayoumi A, Ashby P (1989) Projections of group Ia afferents to motoneurons of thigh muscles in man. Exp Brain Res 76:223–28
Bergui M, Dimanico U, Paglia G, Quattrocolo G, Troni W, Bergamini L (1992) Stretch reflex of quadriceps femoris in normal man: methodological considerations and normative data. Electromyogr Clin Neurophysiol 32:597–601
Bergui M, Paglia G, Lopiano L, Quattrocolo G, Bergamini L, Bergamasco B (1993) Early modification of stretch reflex in Parkinson’s disease. Acta Neurol Scand 88:16–20
Bonnard M, Camus M, Coyle T, Pailhous J (2002) Task-induced modulation of motor evoked potentials in upper-leg muscles during human gait: a TMS study. Eur J Neurosci 16:2225–30
Capaday C, Forget R, Fraser R, Lamarre Y (1991) Evidence for a contribution of the motor cortex to the long-latency stretch reflex of the human thumb. J Physiol 440:243–55
Christensen LO, Andersen JB, Sinkjær T, Nielsen JB (2001) Transcranial magnetic stimulation and stretch reflexes in the tibialis anterior muscle during human walking. J Physiol 531:545–57
Day BL, Riescher H, Struppler A, Rothwell JC, Marsden CD (1991) Changes in the response to magnetic and electrical stimulation of the motor cortex following muscle stretch in man. J Physiol 433:41–57
Dietz V, Discher M, Faist M, Trippel M (1990) Amplitude modulation of the human quadriceps tendon jerk reflex during gait. Exp Brain Res 82:211–13
Engberg I, Lundberg A (1969) An electromyographic analysis of muscular activity in the hindlimb of the cat during unrestrained locomotion. Exp Brain Res 75:614–30
Garland SJ, Gerilovsky L, Enoka RM (1994) Association between muscle architecture and quadriceps femoris H-reflex. Muscle Nerve 17:581–92
Grey MJ, Ladouceur M, Andersen JB, Nielsen JB, Sinkjær T (2001) Group II muscle afferents probably contribute to the medium latency soleus stretch reflex during walking in humans. J Physiol 534:925–33
Hammond PH (1956) The influence of prior instruction to the subject on an apparently involuntary neuromuscular response. J Physiol 182:17–18P
Kearney RE, Stein RB, Parameswaran L (1997) Identification of intrinsic and reflex contributions to human ankle stiffness dynamics. IEEE Trans Biomed Eng 44:493–504
Kurus K., Kitamura J (1999) Long-latency reflexes in contracted hand and foot muscles and their relations to somatosensory evoked potentials and transcranial magnetic stimulation of the motor cortex. Clin Neurophysiol 110:2014–19
Lee RG, Tatton WG (1975) Motor responses to sudden limb displacements in primates with specific CNS lesions and in human patients with motor system disorders. Can J Neurol Sci 2:285–93
Lee RG, Tatton WG (1982) Long latency reflexes to imposed displacements of the human wrist: dependence on duration of movement. Exp Brain Res 45:207–16
Lin DC, Rymer WZ (1993) Mechanical properties of cat soleus muscle elicited by sequential ramp stretches: implications for control of muscle. J Neurophysiol 70:997–1008
Marsden CD, Merton PA, Morton HB (1973) Is the human stretch reflex cortical rather than spinal? Lancet 1:759–61
Marsden CD, Merton PA, Morton HB, Adam J (1977) The effect of lesions of the sensorimotor cortex and the capsular pathways on servo responses from the human long thumb flexor. Brain 100:503–26
Marsden CD, Rothwell JC, Day BL (1983) Long-latency automatic responses to muscle stretch: Origin and function. In: Desmedt JE (eds) Motor Control Mechanisms in Health and Disease. Raven Press, New York, pp 509–39
Matthews PB (1984) Evidence from the use of vibration that the human long-latency stretch reflex depends upon spindle secondary afferents. J Physiol 348:383–415
Matthews PB (1986) Observations on the automatic compensation of reflex gain on varying the pre-existing level of motor discharge in man. J Physiol 374:73–90
Miscio G, Pisano F, Del Conte C, Pianca D, Colombo R, Schieppati M (2001) The shortening reaction of forearm muscles: the influence of central set. Clin Neurophysiol 112:884–94
Mrachacz-Kersting N, Sinkjær T (2003) Reflex and non-reflex torque responses to stretch of the human knee extensors. Exp Brain Res 151:72–81
Mrachacz-Kersting N., Lavoie BA, Andersen JB, Sinkjær T (2004) Characterization of the human quadriceps stretch reflex during human walking. Exp Brain Res 159:108–22
Nashner LM (1976) Adapting reflexes controlling the human posture. Exp Brain Res 26 (1):59–72
Nene A, Byrne C, Hermens H. Is rectus femoris really part of quadriceps? Assessment of rectus femoris function during gait in able-bodied adults. Gait Posture. 2004; Doi:10.1016/S0966-6362(03)00074-2
Nielsen J, Petersen N, Fedirchuk B (1997) Evidence suggesting a transcortical pathway from cutaneous foot afferents to tibialis anterior motoneurons in man. J Physiol 501:473–84
Palmer E, Ashby P (1992) Evidence that a long latency stretch reflex in humans is transcortical. J Physiol 449:429–40
Petersen N, Christensen LO, Morita H, Sinkjær T, Nielsen J (1998) Evidence that a transcortical pathway contributes to stretch reflexes in the tibialis anterior muscle in man. J Physiol 512:267–76
Schieppati M, Nardone A (1997) Medium-latency stretch reflexes of foot and leg muscles analysed by cooling the lower limb in standing humans. J Physiol 503:691–698
Sinkjær T, Toft E, Andreassen S, Hornemann BC (1988) Muscle stiffness in human ankle dorsiflexors: intrinsic and reflex components. J Neurophysiol 60:1110–21
Sinkjaer T, Andersen JB, Nielsen JF, Hansen HJ (1999) Soleus long-latency stretch reflexes during walking in healthy and spastic humans. Clinical Neurophysiology 110:951–59
Thilmann AF, Schwarz M, Topper R, Fellows SJ, Noth J (1991) Different mechanisms underlie the long-latency stretch reflex response of active human muscle at different joints. J Physiol 444:631–43
Toft E, Sinkjær T, Andreassen S, Larsen K (1991) Mechanical and electromyographic responses to stretch of the human ankle extensors. J Neurophysiol 65:1402–10
Van Doornik J, Masakado Y, Sinkjær T, Nielsen JB. The suppression of the long-latency stretch reflex in the human tibialis anterior muscle by transcranial magnetic stimulation. Exp Brain Res 2004; DOI: 10.1007/s00221-004-1966-2
Voigt M, de Zee M, Sinkjær T (1999) A fast servo-controlled hydraulic device for the study of muscle mechanical and reflex properties in humans. In: Herzog W, Jinah A (eds) Proceedings of the 17th Congress of the International Society of Biomechanics; Aug 8–13; Calgary, Canada; pp 578
Wilmink RJH, Nichols TR (2003) Distribution of heterogenic reflexes among the quadriceps and triceps surae muscles of the cat hind limb. J Neurophysiol 90:2310–24
Yang JF, Stein RB, James KB (1991) Contribution of peripheral afferents to the activation of the soleus muscle during walking in humans. Exp Brain Res 87:679–687
Zuur B, Grey MJ, Nielsen JB, Sinkjær T. Supraspinal contributions to the long latency stretch reflex during human walking are different for soleus and tibialis anterior. Program No. 187.23. 2004 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience, 2004. Online
Acknowledgments
This study was funded by The Danish National Research Foundation. The authors would also like to express their gratitude to Mr. Knud Larsen for his valuable technical support.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mrachacz-Kersting, N., Grey, M. & Sinkjær, T. Evidence for a supraspinal contribution to the human quadriceps long-latency stretch reflex. Exp Brain Res 168, 529–540 (2006). https://doi.org/10.1007/s00221-005-0120-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-005-0120-0