Elsevier

NeuroImage

Volume 57, Issue 2, 15 July 2011, Pages 502-512
NeuroImage

Handedness-dependent and -independent cerebral asymmetries in the anterior intraparietal sulcus and ventral premotor cortex during grasp planning

https://doi.org/10.1016/j.neuroimage.2011.04.036Get rights and content

Abstract

When planning grasping actions, right-handers show left-lateralized responses in the anterior intraparietal sulcus (aIPS) and ventral premotor cortex (vPMC), two areas that are also implicated in sensorimotor control of grasp. We investigated whether a similar cerebral asymmetry is evident in strongly left-handed individuals. Fourteen participants were trained to grasp an object appearing in a variety of orientations with their left and right hands and with a novel mechanical tool (operated with either hand). BOLD fMRI data were then acquired while they decided prospectively whether an over- or under-hand grip would be most comfortable for grasping the same stimulus set while remaining still. Behavioral performances were equivalent to those recorded previously in right-handers and indicated reliance on effector-specific internal representations. In left-handers, however, grip selection decisions for both sides (left, right) and effectors (hand, tool) were associated with bilateral increases in activity within aIPS and vPMC. A direct comparison between left- and right-handers did reveal equivalent increases in left vPMC regardless of hand dominance. By contrast, aIPS and right vPMC activity were dependent on handedness, showing greater activity in the motor-dominant hemisphere. Though showing bilateral increases in both left- and right-handers, greater increases in the motor dominant hemisphere were also detected in the caudal IPS (cIPS), superior parietal lobule (SPL) and dorsal premotor cortex (dPMC). These findings provide further evidence that regions involved in the sensorimotor control of grasp also participate in grasp planning, and that for certain areas hand dominance is a predictor of the cerebral organization of motor cognitive functions.

Highlights

► Equivalent effector-specific grip selection behaviors for left- and right-handers ► Equivalent increases in left vPMC regardless of hand dominance ► Increased aIPS and right vPMC activity in the motor-dominant hemisphere ► Hand dominance predicts the cerebral organization of certain motor cognitive functions.

Introduction

The left cerebral hemispheres of the vast majority of humans are dominant for manual sensorimotor control, and this is reflected in their preference for use of the right hand (Kimura and Archibald, 1974). Left cerebral asymmetries are also apparent in neural activity associated with a variety of motor-related cognitive functions including the representation of acquired skills (Johnson-Frey et al., 2005a, Kroliczak and Frey, 2009, Moll et al., 2000, Rumiati et al., 2004), motor imagery (Gerardin et al., 2000), action selection (Rushworth et al., 1998, Schluter et al., 2001), and motor attention (Rushworth et al., 2001, Rushworth et al., 1997). Due to the exclusion of left-handed participants, however, our understanding of the relationship between these cerebral asymmetries and variations in motor dominance is quite limited (Kroliczak et al., 2011). To address this issue, we focus on the motor–cognitive functions involved in planning grasping actions.

There is considerable evidence for similarities between monkeys and humans in the neural organization of grasp (Castiello and Begliomini, 2008, Grafton, 2010). In monkeys, the anterior intraparietal area (AIP) and ventral premotor cortex (F5) (Jeannerod et al., 1995, Sakata et al., 1997) are critically involved in sensory–motor transformations for grasping. In monkeys, AIP and F5 are reciprocally interconnected (Luppino et al., 1999), and a similar pattern of connectivity may exist in humans (Rushworth et al., 2006). Likewise, a growing number of functional neuroimaging studies demonstrate involvement of the human anterior intraparietal sulcus (aIPS), and in some studies ventral premotor cortex (vPMC), in the control of grasp (Binkofski et al., 1999, Binkofski et al., 1998, Culham et al., 2003, Ehrsson et al., 2001, Johnson-Frey et al., 2005b, Kroliczak et al., 2008).

In addition to their involvement in sensorimotor transformations, these inferior posterior parietal and ventral premotor regions also appear to contribute to grasp planning. Macaque AIP (Murata et al., 2000) and F5 (Murata et al., 1997) contain visual neurons that respond selectively to the observation of 3-D shapes even when no hand movements are involved. Effective stimuli are typically of a shape that is compatible with the particular cell's preferred hand configuration, suggesting the possible involvement of these units in the selection of appropriate grasping actions (Murata et al., 1997, Murata et al., 2000). Results from a recent investigation of prospective grip selection in humans are consistent with these observations. When required to select the most comfortable way (over- vs. under-hand) to precision grasp differently oriented objects while remaining still, right-handed humans showed clear behavioral evidence of relying on representations that accurately captured the unique biomechanical properties of the left and right limbs. Importantly, these prospective grip selection decisions were accompanied by left-lateralized increases in aIPS and vPMC regardless of the hand involved (Jacobs et al., 2010). After practice grasping stimuli with a formerly novel handheld tool, participants' prospective grip selection decisions showed evidence of relying on internal representations that captured the unique mechanical and dynamical properties of the instrument (Arbib et al., 2009). Critically, the left aIPS and vPMC again showed increased activity during these decisions. These findings suggest that in addition to their roles in sensorimotor control of grasp, the human left aIPS and vPMC participate in effector-specific grasp planning (Frey, 2010).

Despite apparent similarities in their functional architecture, human grasping behaviors are distinguishable from those exhibited by monkeys in at least two key ways. First, humans demonstrate a strong population-level preference for using their right hands to grasp objects. Interestingly, many left-handers also exhibit a right hand preference in precision grasping tasks (Gonzalez and Goodale, 2009, Gonzalez et al., 2007a). Like right-handers, they are also less affected by visual illusions when grasping objects with their right hands (Gonzalez et al., 2006). These findings have been interpreted as evidence that the left hemisphere is specialized for grasping regardless of hand dominance. However, these predictions are not easily reconciled with recent fMRI findings that indicate bilateral increases in aIPS when right- or left-handers actively grasp objects with either hand (Begliomini et al., 2008). As with many investigations of visually-guided grasping in humans, increases in vPMC were not detected (Castiello and Begliomini, 2008). The aIPS increases were greater in both hemispheres for right- vs. left-handers, but only when using their dominant right hands. Left-handers, by contrast, showed no differences in aIPS activity between hands. One unexplored possibility is that, like right-handers (Jacobs et al., 2010), left-handers might show evidence of a left-cerebral asymmetry in aIPS and vPMC activity during the planning of precision grasping actions.

Second, while extensive training can teach monkeys to grasp with a tool (Umilta et al., 2008), humans flexibly make use of a variety of instruments (e.g., chopsticks, pliers, tweezers, and tongs) when grasping objects in everyday life. As introduced earlier, recent work from our lab with right-handers suggests that through experience the left aIPS and vPMC come to support effector-specific representations involved in planning such tool use behaviors (Jacobs et al., 2010). Whether these areas play a similar role in left-handed individuals is uncertain.

The primary goal of the current investigation is to test the hypothesis that the left hemisphere specialization for motor–cognitive functions observed in right-handed individuals is independent of motor dominance. If so, then we expect that, like right-handers, left-handers will show selective increases in left aIPS and vPMC when performing a prospective grip selection task based on the use of either hand. After training, we predict that these same areas will also show increased activity when planning grasping actions involving use of a formerly novel tool. Alternatively, motor–cognitive functions may be a specialization of the motor dominant hemisphere, as suggested by a recent fMRI investigation of motor imagery in left- and right-handers (Willems et al., 2009). If this is the case, then we expect left-handers to show the opposite pattern of right-handers, i.e., increases in right aIPS and vPMC during prospective grip selection.

Section snippets

Participants

Sixty self-identified left-handed adults gave their informed consent and were administered the Edinburgh Handedness Inventory (Oldfield, 1971). Of these, 16 participants (7 females) with normal or corrected-to-normal visual acuity scored in the top quartile of left-hand dominance (Edinburgh laterality quotient range =−75 to − 100; mean =  89). Two participants were excluded from this study due to an inability to complete all testing sessions. The remaining 14 participants (7 females age range 19–45 

Assessments of hand dominance

Due to technical difficulties, CTs for the 9-hole pegboard task were not recorded for 2 participants. For the remaining 12 participants, differences in mean CTs between the left (M = 17.98, SD = 1.83) vs. right (M = 18.45, SD = 1.15) hands failed to reach significance, t (11) = 1.31, p = .22. This is consistent with observations that the precision grasping behaviors of many left-handed individuals are indistinguishable from those of right-handers (Gonzalez et al., 2007b). By contrast, maximum grip strength

Discussion

Previous work reported left-lateralized increases in the aIPS and vPMC during grip selection judgments involving use of the hands or a recently mastered mechanical tool (Jacobs et al., 2010). The objective of the current investigation was to evaluate whether this left cerebral asymmetry is independent of motor dominance. If so, then we expected a similar pattern for left-handed (i.e., right hemisphere motor dominant) participants. Instead, we found consistent bilateral increases in both the

Acknowledgments

This work has been supported by a grant to S.H.F. from the National Institute of Neurological Disorders and Stroke (NIH/NINDS; # NS053962). S.J. was supported in part by a post-doctoral grant from the Fyssen Foundation. S.J. and S.H.F. designed the experiment. K.M. collected the data. K.M. and S.J. analyzed the data, and S.H.F. and K.M. wrote the manuscript.

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      On a neural level, both groups showed increasing task-related activity in the left PMv and aIPS, but only the training group also showed increasing task-related activity right hemispheric homologous areas implicating the bilateral ventrolateral grasping pathway (Binkofski and Buxbaum, 2013; Rizzolatti and Matelli, 2003). The ventrolateral grasping pathway is involved in the abstract representation of action goals and has been shown to decode goal-directed object manipulation irrespective of whether a hand or a tool was used as end-effector in both, monkeys and humans (Arbib et al., 2009; Gallivan et al., 2013; Garcea and Mahon, 2014; Martin et al., 2011; Ochiai et al., 2005). To the best of our knowledge, we are the first to show that learning novel hand-to-tool transformations is accompanied with bilaterally increasing activity in the ventrolateral grasping pathway over the course of training but many studies have reported activity of the left-hemispheric ventrolateral grasping pathway in a single scanning session.

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    Current address: INSERM Unit 834, Bron, France.

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