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. 2010 Jan 26;20(2):176-81.
doi: 10.1016/j.cub.2009.11.063. Epub 2010 Jan 21.

Causal connectivity between the human anterior intraparietal area and premotor cortex during grasp

Marco Davare  1 , John C Rothwell, Roger N Lemon
Affiliations

Causal connectivity between the human anterior intraparietal area and premotor cortex during grasp

Marco Davare et al. Curr Biol. .

Abstract

The cortical visuomotor grasping circuit, comprising the anterior intraparietal area (AIP), ventral premotor (PMv), and primary motor cortex (M1) allows transformation of an object's physical properties into a suitable motor command for grasp [1-9]. However, little is known about how AIP contributes to the processing of grasp-related information conveyed through the cortical grasping circuit. We addressed this by studying the consequences of AIP "virtual lesions" on physiological interactions between PMv and M1 at rest or during preparation to grasp objects with either a precision grip or a whole-hand grasp. We used a conditioning-test transcranial magnetic stimulation (TMS) paradigm to test how PMv-M1 interactions [10-12] were modified by disrupting AIP function with theta-burst TMS (cTBS) [13]. At rest, AIP virtual lesions did not modify PMv-M1 interactions. In contrast, the usual muscle-specific PMv-M1 interactions that appeared during grasp preparation were significantly reduced following AIP cTBS without directly modifying corticospinal excitability. Behaviorally, disruption of AIP was also associated with a relative loss of the grasp-specific pattern of digit muscle activity. These findings suggest that grasp-related and muscle-specific PMv-M1 interactions are driven by information about object properties provided by AIP.

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Figures

Figure 1
Figure 1
Trifocal Transcranial Magnetic Stimulation and Experimental Task (A) Coil orientations and location of the transcranial magnetic stimulation (TMS) sites as given by neuronavigation; the ventral premotor (PMv) (−56, 13, 18) is shown in blue, the primary motor cortex (M1) (−34, −25, 57) in red, the anterior intraparietal area (AIP) (−43, −39, 46) in green, and the control theta-burst TMS (cTBS) site in yellow. The ellipses show the 95% confidence interval centered over the mean calculated for all subjects (n = 9). See Supplemental Experimental Procedures for details. (B) Experimental task: subjects had to grasp objects at their own pace using either a precision grip between the index and thumb or a whole-hand grasp. A turntable randomly presented the objects 30 cm in front of the subject's hand pad. A screen, made from switchable transparent glass, was positioned between the subject and the turntable to allow precise timing of object presentation. (C) Experimental procedure: subjects performed 3 blocks of 50 trials before and after cTBS over AIP (or over the control area). Objects were presented in a random order, and TMS occurred 800 ms after object presentation (the disc, in this example). The TMS pulse was the go signal for subjects to start moving the hand, which occurred on average 700 ms later (see Supplemental Experimental Procedures). Typical recordings of the first dorsal interosseous (1DI) and abductor digiti minimi (ADM) are shown before and after cTBS over AIP.
Figure 2
Figure 2
Effect of Anterior Intraparietal Area cTBS on PMv-M1 Interactions and on the Muscle Pattern (A) Relative amplitude of motor-evoked potentials (MEPs) (± standard deviation [SD]) recorded from the 1DI and ADM when preparing to grasp either the pen or the disc (left: before cTBS; right: after cTBS). y axis values represent the relative MEP amplitudes resulting from a suprathreshold test (T) stimulus applied over M1 preceded by a subthreshold conditioning (C) stimulus applied over PMv at different C-T intervals (x axis). Note that the facilitation of the 1DI when grasping the pen and of the ADM when grasping the disc (∗p < 0.05) decreased following cTBS (∗∗p < 0.05). (B) Z score normalized electromyographic (EMG) activity (±SD) measured during grasp of the pen or the disc (left: before cTBS; right: after cTBS). EMG activity was measured between the time at which subjects left the hand pad and 100 ms before the object liftoff. The 1DI was more active when grasping the pen compared to the disc and, conversely, the ADM was more active when grasping the disc compared to the pen (∗p < 0.05). Note the less-selective muscle pattern following AIP cTBS (∗∗p < 0.05). (C) Correlation between the effect of AIP cTBS on the MEP size and on the muscle pattern. The axes represent the effect of AIP cTBS in reducing the EMG activity (x axis) and the MEP facilitation (y axis) expressed in percent of values measured before the AIP cTBS. Left: 1DI values when grasping the pen; right: ADM values when grasping the disc. Note that the greater the disruptive effect of cTBS on MEP facilitation, the more the muscle pattern during grasp was disturbed.
Figure 3
Figure 3
Schematic Model of Connectivity between AIP, PMv, and M1 PMv is connected with M1 corticospinal neurons (CSN; black pyramids) via indirect inhibitory (red) and facilitatory (blue) pathways (late I-wave pathways). The PMv output neurons (orange pyramids) giving rise to these pathways receive inhibitory and facilitatory connections from canonical neurons in PMv (orange diamond). Object-related neurons in AIP (green diamond) make facilitatory projections to canonical neurons in PMv. At rest, conditioning TMS over PMv reveals net inhibitory PMv-M1 interactions. When grasping the disc, the corresponding object-related neurons in AIP increase their firing rate, which facilitates in turn the appropriate canonical neurons in PMv. In this example, activation of the PMv canonical cell yields facilitation of the ADM muscle representation by inhibition of the PMv-M1 inhibitory connections and facilitation of the facilitatory PMv-M1 connections.
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