Broca's region subserves imagery of motion: a combined cytoarchitectonic and fMRI study

Abstract

Broca's region in the dominant cerebral hemisphere is known to mediate the production of language but also contributes to comprehension. Here, we report the differential participation of Broca's region in imagery of motion in humans. Healthy volunteers were studied with functional magnetic resonance imaging (fMRI) while they imagined movement trajectories following different instructions. Imagery of right-hand finger movements induced a cortical activation pattern including dorsal and ventral portions of the premotor cortex, frontal medial wall areas, and cortical areas lining the intraparietal sulcus in both cerebral hemispheres. Imagery of movement observation and of a moving target specifically activated the opercular portion of the inferior frontal cortex. A left-hemispheric dominance was found for egocentric movements and a right-hemispheric dominance for movement characteristics in space. To precisely localize these inferior frontal activations, the fMRI data were coregistered with cytoarchitectonic maps of Broca's areas 44 and 45 in a common reference space. It was found that the activation areas in the opercular portion of the inferior frontal cortex were localized to area 44 of Broca's region. These activations of area 44 can be interpreted to possibly demonstrate the location of the human analogue to the so-called mirror neurones found in inferior frontal cortex of nonhuman primates. We suggest that area 44 mediates higher-order forelimb movement control resembling the neuronal mechanisms subserving speech.

Figure 1

Motion trajectory. The double circle displayed on the screen during visually guided finger movements occupied 4° of the visual field of the subject. Performance of the motor and imagery tasks was paced to 0.5 Hz according to prescanning training.

Figure 2

Axial and frontal SPM look‐through projections of the activations in the different behavioural conditions compared with rest. Movement 1 (SG): Somatosensory guided movement. Imagery 1 (SG): Imagery of somatosensory guided movement. Movement 2 (VG): Visually guided movement. Imagery 2 (VG): Imagery of visually guided movement. Imagery 3 (SO): Imagery of self‐observation. Imagery 4 (TO): Imagery of target observation. In all conditions the subjects had their eyes closed except for Movement 3 (VG) and the corresponding control state when the subjects viewed the target on the screen. Right in the images is left in the subjects.

Figure 3

Cytoarchitectonic identification and localisation of area 44. (a) Nissl stained cortex of area 44, arror indicates cytoarchitectonic border to area 47. (b) Localization of area 44 in the inferior frontal cortex in a coronal section of one human brain; prcs = precentral sulcus; ds = diagonal sulcus; cs = central sulcus; pop = pars opercularis of inferior frontal gyrus. (c) Profile of grey matter levels with peak indicative of border between areas 44 and 47.

Figure 4

Intermodal integration of activation and cytoarchitectonic areas on MRI. Superimposition of the inferior frontal activation area (pink) onto cytoarchitectonic area 44: upper row, 67% overlap with mean cytoarchitectonic area during imagery of the moving target, middle row, 45% overlap during imagery of movement observation. Activations compared with rest. Right in the image corresponds to left in the subjects. The degree of spatial overlap of cytoarchitectonic area 44 among the postmortem brains is color coded according to the color bar (1 brain = blue, 10 brains = brown). a = ascending branch of the lateral fissure; h = horizontal branch of the lateral fissure; prc = precentral sulcus; d = diagonal sulcus; lf = lateral fissure; if = inferior frontal sulcus; levels 10 and 20 mm dorsal to the intercommissural line. Lower row, localization of the activated areas on the lateral views of both cerebral hemispheres related to imagery of movement with somatosensory guidance (Imagery 1 SG), visual guidance (Imagery 2 VG), movement observation (Imagery 3 SO), and of the moving target (Imagery 4 TO).