Functional Responses in the Human Spinal Cord during Willed Motor Actions: Evidence for Side- and Rate-Dependent Activity

Abstract

Although the spinal cord is the output station of the central motor system, little is known about the relationships between its functional activity and willed movement parameters in humans. We investigated here blood oxygenation level-dependent functional magnetic resonance imaging (fMRI) signal changes in the cervical spinal cord during a simple finger-to-thumb opposition task in 13 right-handed volunteers, using a dedicated array of 16 receive-only surface coils on a 3 Tesla MRI system. In a first experiment, we found significant fMRI signal increases on both sides of the lower cervical spinal cord while subjects performed the motor task at a comfortable pace (ϳ0.5 Hz) using either hand. Both the spatial extent of movement-related clusters and peak signal increases were significantly higher on the side of the cord ipsilateral to the moving hand than on the contralateral side. Movement-related activity was consistently larger than signal fluctuations during rest. In a second experiment, we recorded spinal cord responses while the same motor sequence was performed using the dominant hand at two different rates (ϳ0.5 or 1 Hz). The intensity but not the spatial extent of the response was larger during higher rates, and it was higher on the ipsilateral side of the cord. Notwithstanding the limited spatial resolving power of the adopted technique, the present results clearly indicate that the finger movement-related fMRI signals recorded from the spinal cord have a neural origin and that as a result of recent technological advances, fMRI can be used to obtain novel and quantitative physiological information on the activity of spinal circuits.

Tactile‐associated fMRI recruitment of the cervical cord in healthy subjects

“…We indeed showed an average signal changes of around 3.2% (range 5 2.8-4.6%), which is consistent with previous findings [Stroman and Ryner, 2001]. Similar findings have been previously reported by spinal cord fMRI studies performed in healthy subjects [Maieron et al, 2007;Stracke et al, 2005;Stroman and Ryner, 2001;Yoshizawa et al, 1996], which showed that both movement [Maieron et al, 2007;Yoshizawa et al, 1996] and tactile stimulation [Stracke et al, 2005;Stroman and Ryner, 2001] of the hand have the potential to elicit cord activity bilaterally, albeit largely in the cord side ipsilateral to the moving/stimulated hand. According to the expected anatomical distribution of the tactile-associated cord recruitment [Brodal, 1981;Kandel et al, 1991;Williams and Warwick, 1980], fMRI activity was predominantly detected on the side of the body being stimulated.…”

“…Despite this, seminal studies have shown that spinal cord fMRI is feasible and enables to obtain reliable results both in healthy subjects [Govers et al, 2007;Komisaruk et al, 2002;Kornelsen and Stroman, 2004;Li et al, 2005;Madi et al, 2001;Maieron et al, 2007;Moffitt et al, 2005;Ng et al, 2006;Stracke et al, 2005;Stroman and Ryner, 2001;Stroman et al, , 2002aStroman et al, , 2003aStroman et al, , 2005aYoshizawa et al, 1996] and in patients with spinal cord injury [Kornelsen and Stroman, 2007;Stroman et al, 2002bStroman et al, , 2004.…”

“…Several spinal cord fMRI studies have examined the regional distribution of cord activity during movements of the upper [Govers et al, 2007;Madi et al, 2001;Maieron et al, 2007;Ng et al, 2006;Yoshizawa et al, 1996] and lower limbs as well as following thermal and painful stimulation of different dermatomes [Moffitt et al, 2005;Stroman et al, 2002aStroman et al, ,b, 2004Stroman et al, , 2005a in healthy subjects, but only a few studies have investigated cord recruitment following a tactile stimulation [Stracke et al, 2005;Stroman et al, 2002a]. The advantages of tactile stimuli for spinal cord fMRI experiments is at least twofold.…”

fMRI Detection of Spinal Activity during Voluntary Movements

“…In experiment 1, clusters of activation were detected on both sides of the spinal cord during the execution of finger taps with either hand [Maieron et al (2007) Although BOLD spinal cord activity that corresponds to stimulated dermatomes or myotomes has been reported previously (Stroman, 2005), the present findings provide compelling evidence regarding the lateralization and the modulation of the spinal neuronal activity as a function of different movement characteristics. The predominant activation of the spinal cord ipsilateral to the hand performing the motor task as well as the greater intensity of the signal at higher levels of voluntary movement parameters indicate that the spinal BOLD signal measured using fMRI results from physiological activity of spinal neurons.…”

“…In a study recently published in The Journal of Neuroscience, Maieron et al (2007) attempt to overcome the methodological hurdles specific to spinal fMRI BOLD imaging and to record activity in the cervical spinal cord while volunteers perform a finger-opposition sequence task either at a fixed frequency, alternating between the left and right hands (experiment 1), or at two different frequencies with the right (dominant) hand only (experiment 2).…”