Excitability at the Motoneuron Pool and Motor Cortex Is Specifically Modulated in Lengthening Compared to Isometric Contractions

Abstract

Neural control of muscle contraction seems to be unique during muscle lengthening. The present study aimed to determine the specific sites of modulatory control for lengthening compared with isometric contractions. We used stimulation of the motor cortex and corticospinal tract to observe changes at the spinal and cortical levels. Motor-evoked potentials (MEPs) and cervicomedullary MEPs (CMEPs) were evoked in biceps brachii and brachioradialis during maximal and submaximal lengthening and isometric contractions at the same elbow angle. Sizes of CMEPs and MEPs were lower in lengthening contractions for both muscles (by approximately 28 and approximately 16%, respectively; P < 0.01), but MEP-to-CMEP ratios increased (by approximately 21%; P < 0.05). These results indicate reduced excitability at the spinal level but enhanced motor cortical excitability for lengthening compared with isometric muscle contractions.

Neural control of lengthening contractions

“…The reduction has been reported both when resisting an imposed force at a constant velocity (Duclay et al, 2011;Gruber et al, 2009) and when lowering an inertial load even with the background EMG activity matched, a method that controls partly for differences in the recruitment gain in the motor neurone pool (Pierrot-Deseilligny and Burke, 2012), during both types of anisometric contractions with the elbow flexor (Abbruzzese et al, 1994;Sekiguchi et al, 2001) and soleus (Sekiguchi et al, 2003) muscles. With this approach, MEP amplitude is reduced in the soleus during a maximal lengthening contraction of the plantar flexors compared with a maximal shortening contraction ( Fig.…”

“…The tension-regulating inhibitory hypothesis An often-evoked suggestion for the lower voluntary activation during maximal lengthening contractions is the intervention of a tension-regulating mechanism intended to protect the muscletendon unit against excessive tension (Amiridis et al, 1996;Del Valle and Thomas, 2005;Gruber et al, 2009;Seger and Thorstensson, 2000;Westing et al, 1990Westing et al, , 1991. Despite earlier animal and human experiments having shown that the Golgi tendon organs (Ib inhibition; see Houk and Henneman, 1967;Priori et al, 1998) are not responsible for the 'clasp-knife' phenomenon triggered at high muscle forces (Rymer et al, 1979), the proponents of this protective strategy assume that the inhibitory action of the Golgi tendon organs is to depress the responsiveness of the motor neurones, thereby limiting the force produced by the muscle-tendon unit.…”

“…With the exception of the work by Hahn and colleagues (2012), most studies have found that a greater brain area is involved in the control of lengthening contractions than other types of contractions regardless of load type (inertial load or torque motor). The greater responsiveness of the motor cortex during lengthening contractions has been interpreted as indicating extra excitatory descending drive to compensate for spinal inhibition (Gruber et al, 2009). It is uncertain whether such modulation involves the activation of different cortical areas during lengthening and shortening contractions, as suggested by functional MRI (Kwon and Park, 2011) and by the selective modulation of descending pathways mediating spinal presynaptic inhibition during lengthening contractions but not during isometric and shortening contractions (Grosprêtre et al, 2014).…”

“…The greater decrease in the amplitude of the CMEP elicited by electrical stimulation of the cervicomedullary junction relative to the MEP evoked by TMS during lengthening contractions has been attributed to mechanisms that influence the input and output at the motor neurone level (Gruber et al, 2009). Various presynaptic and postsynaptic mechanisms of the motor neurone may contribute to the reduction in responsiveness during lengthening contractions.…”

Intracortical Inhibition Assessed with Paired-Pulse Transcranial Magnetic Stimulation is Modulated during Shortening and Lengthening Contractions in Young and Old Adults

“…This includes observations that voluntary activation, electromyography (EMG), force generation and spinal motoneuron excitability are all different during lengthening contractions [1,2]. Furthermore, recent evidence from studies using a range of neurophysiological and neuroimaging techniques have provided compelling support for distinct patterns of cortical activity during lengthening contractions [3][4][5][6][7][8][9][10][11]. In addition, lengthening contractions are also associated with reduced motor performance [12][13][14].…”