Amplification of interlimb reflexes evoked by stimulating the hand simultaneously with conditioning from the foot during locomotion

BMC Neuroscience

E Paul Zehr³  Tomoyoshi Komiyama⁴  Taryn Klarner²  Trevor Barss²  Tsuyoshi Nakajima¹ 

[1] Department of Integrative Physiology, Kyorin University School of Medicine, 6-20-2 Shinkawa, Mitaka, Japan;Rehabilitation Neuroscience Laboratory, University of Victoria, PO Box 3010 STN CSC, V8W 3P1, Victoria, BC, Canada;School of Exercise Science, Physical, and Health Education, University of Victoria, Victoria, BC, Canada;Department of Health and Sports Sciences, Faculty of Education, Chiba University, Chiba, Japan

关键词: Arm swing;    Cycling;    Walking;    Rehabilitation;    Afferent feedback;    Central pattern generator;    Propriospinal;    Interlimb;    Reflex;   

Others  :  1140387
DOI  :  10.1186/1471-2202-14-28

 received in 2012-12-07, accepted in 2013-03-07,  发布年份 2013

【 摘 要 】

Background

Widespread interlimb reflexes evoked in leg muscles by cutaneous stimulation of the hand are phase-modulated and behaviorally relevant to produce functional changes in ankle trajectory during walking. These reflexes are complementary to the segmental responses evoked by stimulation at the ankle. Despite differences in the expression of reflex amplitude based upon site of nerve stimulation, there are some common features as well, suggesting the possibility of shared interneuronal pathways. Currently little is known about integration or shared reflex systems from interlimb cutaneous networks during human locomotion. Here we investigated convergent reflex effects following cutaneous stimulation of the hand and foot during arm and leg cycling (AL) by using spatial facilitation. Participants performed AL cycling and static activation of the target muscle knee extensor vastus lateralis (VL) in 3 different randomly ordered nerve stimulation conditions: 1) superficial radial nerve (SR; input from hand); 2) superficial peroneal nerve (SP; input from foot); and, 3) combined stimulation (SR + SP). Stimuli were applied around the onset of rhythmic EMG bursts in VL corresponding to the onset of the power or leg extension phase.

Results

During AL cycling, small inhibitory (~80 ms) and large facilitatory reflexes (~100 ~ 150 ms) were seen in VL. The amplitudes of the facilitatory responses with SR + SP stimulation were significantly larger than those for SP or SR stimulation alone. The facilitation was also significantly larger than the simple mathematical summation of amplitudes from SP and SR trials. This indicates extra facilitation beyond what would be accounted for by serial neuronal processing and was not observed during static activation.

Conclusions

We conclude that AL cycling activates shared interneurons in convergent reflex pathways from cutaneous inputs innervating the hand and leg. This enhanced activity has functional implications for corrective responses during locomotion and for translation to rehabilitation after neurotrauma.

【 授权许可】

   
2013 Nakajima et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Zehr EP, Balter JE, Ferris DP, Hundza SR, Loadman PM, Stoloff RH: Neural regulation of rhythmic arm and leg movement is conserved across human locomotor tasks. J Physiol 2007, 582:209-227.
• [2]Zehr EP, Hundza SR, Vasudevan EV: The quadrupedal nature of human bipedal locomotion. ExercSport SciRev 2009, 37(2):102-108.
• [3]Zehr EP, Duysens J: Regulation of arm and leg movement during human locomotion. Neuroscientist 2004, 10(4):347-361.
• [4]Dietz V: Do human bipeds use quadrupedal coordination? Trends Neurosci 2002, 25(9):462-467.
• [5]Dietz V: Quadrupedal coordination of bipedal gait: implications for movement disorders. J Neurol 2011, 258(8):1406-1412.
• [6]Haridas C, Zehr EP: Coordinated interlimb compensatory responses to electrical stimulation of cutaneous nerves in the hand and foot during walking. J Neurophysiol 2003, 90:2850-2861.
• [7]Sakamoto M, Endoh T, Nakajima T, Tazoe T, Shiozawa S, Komiyama T: Modulations of interlimb and intralimb cutaneous reflexes during simultaneous arm and leg cycling in humans. Clin Neurophysiol 2006, 117(6):1301-1311.
• [8]Wannier TMJ, Bastiaanse CM, Columbo G, Dietz V: Arm to leg coordination in humans during walking, creeping and swimming activities. Exp Brain Res 2001, 141:375-379.
• [9]Frigon A, Collins DF, Zehr EP: Effect of rhythmic arm movement on reflexes in the legs: modulation of soleus H-reflexes and somatosensory conditioning. J Neurophysiol 2004, 91(4):1516-1523.
• [10]Zehr EP, Hoogenboom N, Frigon A, Collins DF: Facilitation of soleus H-reflex amplitude evoked by cutaneous nerve stimulation at the wrist is not suppressed by rhythmic arm movement. Exp Brain Res 2004, 159(3):382-388.
• [11]Zehr EP, Klimstra M, Dragert K, Barzi Y, Bowden MG, Javan B, Phadke C: Enhancement of Arm and Leg locomotor coupling with augmented cutaneous feedback from the hand. J Neurophysiol 2007, 98(3):1810-1814.
• [12]Nakajima T, Kitamura T, Kamibayashi K, Komiyama T, Zehr EP, Hundza SR, Nakazawa K: Robotic-assisted stepping modulates monosynaptic reflexes in forearm muscles in the human. J Neurophysiol 2011, 106:1679-1680.
• [13]Sasada S, Tazoe T, Nakajima T, Zehr EP, Komiyama T: Effects of Leg pedaling on early latency cutaneous reflexes in upper limb muscles. J Neurophysiol 2010, 104(1):210-217.
• [14]Balter JE, Zehr EP: Neural coupling between the arms and legs during rhythmic locomotor-like cycling movement. J Neurophysiol 2007, 97(2):1809-1818.
• [15]Mezzarane R, Klimstra M, Lewis A, Hundza S, Zehr E: Interlimb coupling from the arms to legs is differentially specified for populations of motor units comprising the compound H-reflex during “reduced” human locomotion. Experimental Brain Res 2011, 208(2):157-168.
• [16]Falgairolle M, de Seze M, Juvin L, Morin D, Cazalets JR: Coordinated network functioning in the spinal cord: An evolutionary perspective. J Physiology-Paris 2006, 100(5–6):304-316.
• [17]Juvin L, Simmers J, Morin D: Propriospinal circuitry underlying interlimb coordination in mammalian quadrupedal locomotion. J Neurosci 2005, 25(25):6025-6035.
• [18]Sakamoto M, Tazoe T, Nakajima T, Endoh T, Shiozawa S, Komiyama T: Voluntary changes in leg cadence modulate arm cadence during simultaneous arm and leg cycling. Experimental Brain Res 2007, 176(1):188-192.
• [19]Sherrington CS: Flexion-reflex of the limb, crossed extension reflex, and reflex stepping and standing. JPhysiol 1910, 40:28-121.
• [20]Sherrington CS, Laslett EE: Observations on some spinal reflexes and the interconnection of spinal segments. JPhysiol 1903, 29:58-96.
• [21]Lloyd DPC: Mediation of descending long spinal reflex activity. JNeurophysiol 1942, 5:435-458.
• [22]Lundberg A, Malmgren K, Schomburg ED: Convergence from Lb, cutaneous and joint afferents in reflex pathways to motoneurones. Brain Res 1975, 87(1):81-84.
• [23]Baldiserra F, Hultborn H, Illert M: Integration in spinal neuronal systems. In Handbook of physiology. Edited by Brooks VB. Bethesda, MD: Physiol. Soc; 1981:509-595.
• [24]LaBella LA, McCrea DA: Evidence for restricted central convergence of cutaneous afferents on an excitatory reflex pathway to medial gastrocnemius motoneurons. J Neurophysiol 1990, 64:403-412.
• [25]Kagamihara Y, Hayashi A, Masakado Y, Kouno Y: Long-loop reflex from arm afferents to remote muscles in normal man. Experimental Brain Res 2003, 151:136-144.
• [26]Christensen LO, Morita H, Petersen N, Nielsen J: Evidence suggesting that a transcortical reflex pathway contributes to cutaneous reflexes in the tibialis anterior muscle during walking in man. Experimental Brain Res 1999, 124:59-68.
• [27]Lundberg A: Multisensory control of spinal reflex pathways. Prog Brain Res 1979 1979, 50:11-28.
• [28]Zehr EP, Collins DF, Chua R: Human interlimb reflexes evoked by electrical stimulation of cutaneous nerves innervating the hand and foot. Experimental Brain Res 2001, 140:495-504.
• [29]Calancie B, Lutton S, Broton JG: Central nervous system plasticity after spinal cord injury in man: interlimb reflexes and the influence of cutaneous stimulation. Electroencephalogr Clin Neurophysiol 1996, 101(4):304-315.
• [30]Falgairolle M, de Seze M, Juvin L, Morin D, Cazalets JR: Coordinated network functioning in the spinal cord: an evolutionary perspective. J Physiology-Paris 2007. In Press, Corrected Proof
• [31]Lamont EV, Zehr EP: Task-specific modulation of cutaneous reflexes expressed at functionally relevant gait cycle phases during level and incline walking and stair climbing. Exp Brain Res 2006, 173(1):185-192.
• [32]Lamont EV, Zehr EP: Earth-referenced handrail contact facilitates interlimb cutaneous reflexes during locomotion. J Neurophysiol 2007, 98(1):433-442.
• [33]Borgmann A, Hooper SL, Büschges A: Sensory feedback induced by front-Leg stepping entrains the activity of central pattern generators in caudal segments of the stick insect walking system. J Neurosci 2009, 29(9):2972-2983.
• [34]Kawashima N, Nozaki D, Abe MO, Nakazawa K: Shaping appropriate locomotive motor output through interlimb neural pathway within spinal cord in humans. JNeurophysiol 2008, 99(6):2946-2955.
• [35]Zehr EP, Loadman PM: Persistence of locomotor-related interlimb reflex networks during walking after stroke. Clin Neurophysiol 2012, 123(4):796-807.