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A distributed left hemisphere network active during planning of everyday tool use skills - PubMed

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A distributed left hemisphere network active during planning of everyday tool use skills

Scott H Johnson-Frey et al.

Cereb Cortex.

2005 Jun.

Abstract

Determining the relationship between mechanisms involved in action planning and/or execution is critical to understanding the neural bases of skilled behaviors, including tool use. Here we report findings from two fMRI studies of healthy, right-handed adults in which an event-related design was used to distinguish regions involved in planning (i.e. identifying, retrieving and preparing actions associated with a familiar tools' uses) versus executing tool use gestures with the dominant right (experiment 1) and non-dominant left (experiment 2) hands. For either limb, planning tool use actions activates a distributed network in the left cerebral hemisphere consisting of: (i) posterior superior temporal sulcus, along with proximal regions of the middle and superior temporal gyri; (ii) inferior frontal and ventral premotor cortices; (iii) two distinct parietal areas, one located in the anterior supramarginal gyrus (SMG) and another in posterior SMG and angular gyrus; and (iv) dorsolateral prefrontal cortex (DLFPC). With the exception of left DLFPC, adjacent and partially overlapping sub-regions of left parietal, frontal and temporal cortex are also engaged during action execution. We suggest that this left lateralized network constitutes a neural substrate for the interaction of semantic and motoric representations upon which meaningful skills depend.

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Figures

Figure 1.

Experimental design for experiments 1 and 2. All stimuli were presented aurally and subjects' eyes remained closed throughout testing. On half of the trials the instructional cue (IC) identified a familiar tool commonly used unimanually with the dominant hand, on the remaining control trials subjects heard the word ‘move’. ICs were immediately followed by a variable duration delay interval during which the associated actions were planned. In control trials subjects prepared a non-meaningful hand movement. A movement cue (MC) instructed subjects to execute (GO) or abort (NOGO) the planned action.

Figure 2.

Activations associated with planning and executing right hand tool use gestures. (A) When compared with preparing random hand movements (CONTROLNOGO condition), planning tool use gestures for the right hand (TOOL-NOGO) is associated with major activations in posterior parietal cortex, posterior temporal, inferior-middle frontal cortices and DLFPC all within the left cerebral hemisphere. (B) Gesture execution involves similar regions as well as a number of other cortical and subcortical structures associated with sensory and motor processes in both hemispheres. Note the strong activation present in contralateral left sensorimotor cortex. See text for details.

Figure 3.

Percent signal change at locations of peak activity in temporal, frontal, and parietal areas during right hand gesture planning. Panels illustrate percent signal change for each condition in data extracted from the locations of peak activity in left posterior temporal (A), inferior frontal (B), anterior SMG (C) and posterior SMG--ANG (D). Data are averaged over a 10 s (4TR) epoch time-locked to the IC onset (see Method for details).

Figure 4.

Major anatomical divisions of posterior parietal cortex in an individual subject. For purposes of localizing activations in individual subjects, boundaries between SPL (green), SMG (yellow) and ANG (purple) were determined on the basis of anatomical landmarks in each subjects' high-resolution, T1-weighted, anatomical MRI scan. This is necessary due to often substantial variations in cortical topography amongst subjects. Placement of borders between parietal and temporal and occipital lobes was based on Duvernoy (1991). Major sulci are drawn in red.

Figure 5.

Activations associated with planning and executing left hand tool use gestures. (A) Consistent with the results of experiment 1, planning tool use gestures for the left hand (TOOL-NOGO versus CONTROL-NOGO comparison) is associated with major activations in left posterior temporal, inferior frontal and posterior parietal cortices, as well as DLFPC. (B) Gesture execution involves similar regions as well as a number of cortical and subcortical structures in both the right and left cerebral hemispheres. Note the strong contralateral activation in right sensorimotor cortex when gestures are planned for execution with the left hand. See text for details.

Figure 6.

Percent signal change at locations of peak activity in temporal, frontal and parietal areas during left hand gesture planning. Panels show percent signal change for each condition in data extracted from regions of peak activity in left posterior temporal (A), inferior frontal (B) and posterior parietal cortices (C, D). The same procedure as described in Figure 3 was used.

Figure 7.

Areas activated when planning and/or executing tool use gestures with the right (experiment 1) and left (experiment 2) hands. Green areas were significantly activated (P < 0.01, K ≥ 10 voxels in both experiments 1 and 2) when executing tool use gestures the right and left hands (TOOL-GO, TOOL-NOGO). Red areas were activated when planning tool use gestures for both the right and left hands (TOOL-NOGO, CONTROL-NOGO). Blue areas were activated when planning and executing tool use gestures with the left and right hands. While bilateral regions of frontal, parietal and temporal cortex are all involved in gesture execution, planning is associated primarily with activations in the left cerebral hemisphere (A). There is both segregation and some degree of overlap amongst regions in left inferior frontal, inferior parietal and posterior temporal cortex that contribute to planning and execution of tool use gestures. Left DLFPC and right STS activity is only observed during gesture planning. Yellow lines on coronal slices (left) indicate dorso-ventral locations (z) of axial slices through key regions contributing to gesture planning and/or execution: posterior temporal cortex (B), inferior frontal cortex (C) and posterior parietal cortex (D). Numbers below coronal slices indicate slice positions along the rostro-caudal (y) axis and those beneath axial slices indicate slice positions along the dorso-ventral (z) axis.