Finger and face representations in the ipsilateral precentral motor areas in humans

Abstract

Several human neuroimaging studies have reported activity in the precentral gyrus (PcG) ipsilateral to the side of hand movements. This activity has been interpreted as the part of the primary motor cortex (M1) that controls bilateral or ipsilateral hand movements. To better understand hand ipsilateral-PcG activity, we performed a functional MRI experiment in eight healthy right-handed adults. Behavioral tasks involved hand or lower face movements on each side or motor imagery of the same movements. Consistent with the known M1 organization, the hand contralateral-PcG activity was centered at the "hand-knob" portion of the PcG; face contralateral-PcG activity was localized ventrolateral to it. Hand ipsilateral-PcG activity was identified in most subjects. However, converging results indicated that this ipsilateral PcG activity was situated in Brodmann's area 6 in both hemispheres. The hand ipsilateral-PcG zones were active not only during hand movements but also face movements. Moreover, the hand ipsilateral-PcG zones revealed substantial imagery-related activity, which also failed to differentiate the hand and face. Statistical analyses confirmed poor effector selectivity of the hand ipsilateral PcG activity during both movement and imagery tasks. From these results, we conclude that the hand ipsilateral-PcG activity in healthy adults probably corresponds to a part of the ventral premotor cortex. In contrast, available evidence suggests that M1 contributes to controlling the ipsilateral hand in children and patients after stroke recovery. It appears that within the human PcG, there are two parallel systems potentially capable of controlling ipsilateral hand movements: ventral premotor cortex and M1. These two systems may be differentially influenced by developmental or pathologic changes.

Fig. 1. Experimental paradigm

In the auditory (A)-visual (V) condition, an auditory stimulus specifying the effector (right hand, left hand, right face or left face) was presented first. After a variable delay period (12~20 s), subjects moved the specified body part or imagined it moving in response to a green (G) or red (R) visual stimulus, respectively. In the visual-auditory condition, a green or red color stimulus was presented first. After a delay period, an auditory stimulus prompted subjects to move the instructed body part or imagine it moving. For example, right hand movement (RH move) should occur in response to the visual stimulus (G) in the auditory-visual condition and to the auditory stimulus (right hand) in the visual-auditory condition.

Fig. 2

Brain activity during right hand movement (A), left hand movement (B), right face movement (C), and left face movement (D) from a conjunction analysis in a representative subject. The contralateral PcG activity and ipsilateral PcG activity are indicated by the cyan and magenta arrows, respectively. Ipsilateral activities anterior to the precentral hand-knob at z = 62 mm (green arrows in A and B) are located in the depth of the precentral sulcus and should beregarded as the dorsal premotor cortex (See Methods for clarification). (E) The areas encompassed by the white squares at z = 44 mm in (A)–(D) are magnified and overlaid for each hemisphere. The hand ipsi-PcG activity (magenta) and face contra-PcG activity (cyan) are shown. The areas in white indicate the ‘ipsilateral parietal’ activity. The coordinates are based on the Montreal Neurological Institute template. The right side of the brain (R) is shown in the right side of the images. L, left; A, anterior (= rostral); P, posterior (= caudal); CS, central sulcus; PcS, precentral sulcus

Fig. 3

A vectorial presentation of the hand ipsi-PcG location in the left (A) and right (B) hemispheres. The hand ipsi-PcG vector (black) and the M1 vector (gray) indicate the direction of the hand ipsi-PcG activity and the face contra-PcG activity, respectively. These vectors are computed in reference to the hand contra-PcG activity as the origin (closed circle). The vectors are projected onto the caudal-rostral (y) and ventral-dorsal (z) plane for presentation. The data are not presented for the medial-lateral axis (x). The scale is in millimeters.

Fig. 4

Somatotopy represented in the PcG zones during the auditory-cued movement (dark gray) and auditory-cued motor imagery (light gray). The contra- and ipsi-PcG zones (See Table 1 for the information) were determined for each effector in each individual. Task-related percent signal changes were averaged across subjects. Error bars represent standard errors of mean. RH, right hand; LH, left hand ; RF, right face; LF, left face

Fig. 5

A possible scheme for the ipsilateral motor systems originating from the PcG. Both premotor cortex and M1 may control the ipsilateral hand below age 10 (childhood). The ipsilateral M1 function is gradually suppressed in the course of the normal development of inhibitory systems such as the transcallosal inhibition from the contralateral M1. In normal adults, only the premotor cortex usually controls ipsilateral or bilateral distal limb movements (adulthood). Withdrawal of the inhibitory inputs due to acquired lesions might lead to the reemergence of ipsilateral M1 function (pathologic).