INTRODUCTION Recording of neural activity during grasping actions [1] in macaques showed that grasp-related sensorimotor transformations are accomplished in a circuit constituted by the anterior part of the intraparietal sulcus (AIP), the ventral (F5) and the dorsal (F2) part of the premotor area [2]. AIP may furnish area F5 with visual signals of objects to aid the selection of grasp configurations appropriate for their attributes. Then F5 provides grasp-related information to F2, which monitors hand configuration while the object is approached [2–4]. In humans, neuroimaging studies have revealed the existence of a similar circuit, involving the putative homolog of macaque areas AIP, F5 and F2 [5-6]. These studies, however, have so far mainly focused on grasping movements of the right hand in right-handers participants, while a few results [7-8] show that brain activation during grasping is not always contralateral to the hand. This suggests that hand preference in grasping could not follow the usual asymmetry in relation to handedness. In addition, the role of the cerebellum of visually guided grasping in relation to handedness has yet to be properly addressed. METHODS A functional resonance imaging experiment (fMRI) has been conducted. Participants: 19 right-handed (RD) and 15 left-handed (LD) participants were tested. Handedness was assessed by using the Edinburg Handedness Inventory [9]. Task and setup: spherical plastic objects (Ø: 3 and 6 cm) were presented in the scanner by means of a metal-free structure. Participants had to grasp (either with right –RH- or left hand -LH) the small object with a precision grip (PG) and the large object with a whole-hand grasp (WHG), according to an acoustic go-signal presented through pneumatic headphones. The head was tilted at an angle (30°) to permit direct viewing of stimuli. Experimental design: an event-related design with Inter-Stimulus-Interval (ISI) varying from 3 to 8 [10] was adopted. Handedness (LD or RD) was the between-subjects factor, while hand (LH or RH) and grasp type (PG or WHG) were the within-subjects factors. Hand was randomized across runs and grasp type was randomized across trials. Imaging parameters: 3T scanner (Siemens Magnetom Trio) with a standard Siemens 12 channels coil was used to acquire images. Functional images: T2*-weighted sequence (47 contiguous axial slices, descending interleaved sequence, 64x64 voxels, 3.3*3.3*3 mm, TE= 3 s, FOV= 2106210 mm2, FA = 90°, TE= 30 ms, bandwidth:1954 Hz/Px). Structural images: T1-weighted images were acquired for each subject (3D MP-RAGE, 176 axial slices, data matrix 256x256, 1 mm isotropic voxels, TR= 1859 ms, TE= 3.14 ms, flip angle= 22°). Analysis: performed using SPM5. First-level analysis was conducted by using a GLM in which regressors were defined on the timing of presentation of the acoustic go-signal for each experimental condition. Functions were convolved with a canonical synthetic HRF and its first-order temporal derivative to produce individual models. The resulting contrasts were entered into a second-level RFX analysis. Analysis focussed on the specific contribution of the grasping circuit to the control of movements performed with either hands in both RD and LD. Therefore a mask involving key areas (AIP, vPMC, dPMC plus the cerebellum and primary motor cortex, M1) was adopted as a searching area for a Small Volume Correction [11]. RESULTS Main effect of hand: main effect of hand was evident within the left M1 and the right lobule for the contrast RH>LH, and in the right M1 and dPMC plus the left cerebellar lobule for the contrast LH>RH. Main effect of handedness: main effect of hand was evident within the left M1 and the right cerebellar lobule for the contrast RD>LD. The opposite contrast LD>RD did not give any significant result. Main effect of grasp type: main effect of grasp type was evident within AIP (bilaterally) for the contrast PG>WHG. The opposite contrast WHG>PG did not give any significant result. Interaction hand x handedness: significant interaction between hand and handedness was evident in the right cerebellum. The activation pattern observed within this area shows no differences in the use of LH between RD and LD, while RD show significantly stronger activity than LD while using RH. Interaction handedness x grasp type: no significant results. Interaction hand x grasp type: significant interaction between hand and grasp type was evident within several areas of both cerebellar lobules, the right dPMC and AIP (bilaterally). Cerebellar lobules and AIP showed a similar pattern, that is no differences in the use of LH between RD and LD, while RD show significantly stronger activity than LD while using RH. The right dPMC shows the opposite pattern, that is no differences between LD and RD when using RH, but significant stronger activity for LD than RD when using LH. Interaction hand x handedness x grasp type: no significant results CONCLUSIONS The results obtained by this study shows that both right- and left-handers seems to prefer the right hand when a skilled grasping movement, such as PG, has to be performed. Moreover, the right dPMC seems to play a fundamental role in monitoring the configuration of fingers when grasping movements are performed, by either the right and the left hand. This role becomes particularly evident when the hand less-skilled to perform such action is utilized. In addition, our results offer some indirect evidence in humans of the connections between the cerebellum and AIP, an area which is fundamental for the visuomotor transformations underlying grasping. Further studies are required to properly understand the role played by hand dominance on the contribution of key areas involved in the control of visually guided grasping.

GRASPING-RELATED ACTIVITY IN THE HUMAN BRAIN: THE ROLE OF HAND AND HANDEDNESS

BEGLIOMINI, CHIARA;CASTIELLO, UMBERTO
2010

Abstract

INTRODUCTION Recording of neural activity during grasping actions [1] in macaques showed that grasp-related sensorimotor transformations are accomplished in a circuit constituted by the anterior part of the intraparietal sulcus (AIP), the ventral (F5) and the dorsal (F2) part of the premotor area [2]. AIP may furnish area F5 with visual signals of objects to aid the selection of grasp configurations appropriate for their attributes. Then F5 provides grasp-related information to F2, which monitors hand configuration while the object is approached [2–4]. In humans, neuroimaging studies have revealed the existence of a similar circuit, involving the putative homolog of macaque areas AIP, F5 and F2 [5-6]. These studies, however, have so far mainly focused on grasping movements of the right hand in right-handers participants, while a few results [7-8] show that brain activation during grasping is not always contralateral to the hand. This suggests that hand preference in grasping could not follow the usual asymmetry in relation to handedness. In addition, the role of the cerebellum of visually guided grasping in relation to handedness has yet to be properly addressed. METHODS A functional resonance imaging experiment (fMRI) has been conducted. Participants: 19 right-handed (RD) and 15 left-handed (LD) participants were tested. Handedness was assessed by using the Edinburg Handedness Inventory [9]. Task and setup: spherical plastic objects (Ø: 3 and 6 cm) were presented in the scanner by means of a metal-free structure. Participants had to grasp (either with right –RH- or left hand -LH) the small object with a precision grip (PG) and the large object with a whole-hand grasp (WHG), according to an acoustic go-signal presented through pneumatic headphones. The head was tilted at an angle (30°) to permit direct viewing of stimuli. Experimental design: an event-related design with Inter-Stimulus-Interval (ISI) varying from 3 to 8 [10] was adopted. Handedness (LD or RD) was the between-subjects factor, while hand (LH or RH) and grasp type (PG or WHG) were the within-subjects factors. Hand was randomized across runs and grasp type was randomized across trials. Imaging parameters: 3T scanner (Siemens Magnetom Trio) with a standard Siemens 12 channels coil was used to acquire images. Functional images: T2*-weighted sequence (47 contiguous axial slices, descending interleaved sequence, 64x64 voxels, 3.3*3.3*3 mm, TE= 3 s, FOV= 2106210 mm2, FA = 90°, TE= 30 ms, bandwidth:1954 Hz/Px). Structural images: T1-weighted images were acquired for each subject (3D MP-RAGE, 176 axial slices, data matrix 256x256, 1 mm isotropic voxels, TR= 1859 ms, TE= 3.14 ms, flip angle= 22°). Analysis: performed using SPM5. First-level analysis was conducted by using a GLM in which regressors were defined on the timing of presentation of the acoustic go-signal for each experimental condition. Functions were convolved with a canonical synthetic HRF and its first-order temporal derivative to produce individual models. The resulting contrasts were entered into a second-level RFX analysis. Analysis focussed on the specific contribution of the grasping circuit to the control of movements performed with either hands in both RD and LD. Therefore a mask involving key areas (AIP, vPMC, dPMC plus the cerebellum and primary motor cortex, M1) was adopted as a searching area for a Small Volume Correction [11]. RESULTS Main effect of hand: main effect of hand was evident within the left M1 and the right lobule for the contrast RH>LH, and in the right M1 and dPMC plus the left cerebellar lobule for the contrast LH>RH. Main effect of handedness: main effect of hand was evident within the left M1 and the right cerebellar lobule for the contrast RD>LD. The opposite contrast LD>RD did not give any significant result. Main effect of grasp type: main effect of grasp type was evident within AIP (bilaterally) for the contrast PG>WHG. The opposite contrast WHG>PG did not give any significant result. Interaction hand x handedness: significant interaction between hand and handedness was evident in the right cerebellum. The activation pattern observed within this area shows no differences in the use of LH between RD and LD, while RD show significantly stronger activity than LD while using RH. Interaction handedness x grasp type: no significant results. Interaction hand x grasp type: significant interaction between hand and grasp type was evident within several areas of both cerebellar lobules, the right dPMC and AIP (bilaterally). Cerebellar lobules and AIP showed a similar pattern, that is no differences in the use of LH between RD and LD, while RD show significantly stronger activity than LD while using RH. The right dPMC shows the opposite pattern, that is no differences between LD and RD when using RH, but significant stronger activity for LD than RD when using LH. Interaction hand x handedness x grasp type: no significant results CONCLUSIONS The results obtained by this study shows that both right- and left-handers seems to prefer the right hand when a skilled grasping movement, such as PG, has to be performed. Moreover, the right dPMC seems to play a fundamental role in monitoring the configuration of fingers when grasping movements are performed, by either the right and the left hand. This role becomes particularly evident when the hand less-skilled to perform such action is utilized. In addition, our results offer some indirect evidence in humans of the connections between the cerebellum and AIP, an area which is fundamental for the visuomotor transformations underlying grasping. Further studies are required to properly understand the role played by hand dominance on the contribution of key areas involved in the control of visually guided grasping.
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