Parietal updating of limb posture: An event-related fMRI study
Introduction
The posterior parietal cortex (PPC) is thought to play a key role in the representation of corporeal and peripersonal space, and in the sensorimotor transformations associated with goal-directed movements (for reviews see Andersen, Snyder, Bradley, & Xing, 1997; Rizzolatti, Fogassi, & Gallese, 1997; Snyder, 2000). In humans damage to the PPC leads to disorders in the representation of space (e.g., hemispatial neglect) and impairments in the planning and control goal-directed movements (e.g., ideomotor limb apraxia and optic ataxia) (Balint, 1909, Critchley, 1953; De Renzi, 1982; Jackson, Newport, Mort, & Husain, 2005; Liepmann & Maas, 1907; Sirigu et al., 1996). Understanding the nature of the sensorimotor transformations carried out by human PPC is a fundamental problem for neuroscience and of considerable clinical importance in treating the consequences of stroke, and other neurological disorders that affect this brain region.
To execute goal-directed movements, such as reaching to pick up an object, information specified in extrinsic (spatial) coordinates must be transformed into a motor plan that can be expressed within intrinsic (motor) coordinates. For reaching movements directed to visually defined targets, this will involve translating visual information that is coded initially in retinotopic coordinates, into a motor plan that specifies the sequence of postural changes required to bring the hand to the target. Electrophysiological and lesion studies in the monkey indicate that there is no single, supramodal, map of space that is used to guide movements. Instead, movements appear to be capable of being planned and controlled within multiple coordinate systems, each one attached to a different body part (see Andersen et al., 1997, Buneo and Andersen, 2006; Gross & Graziano, 1995). Thus, recordings in the superior parietal lobule (SPL) of the monkey brain have demonstrated the existence of a ‘parietal reach region’ (PRR) in which the targets of reaching movements are represented within eye-centred rather than body-centred coordinates (Batista, Buneo, Snyder, & Andersen, 1999). By contrast, other regions of PPC, such as area 5 or area 7b, have few visual inputs, are strongly interconnected with somatosensory and motor cortices, are dominated by somatic and motor responses, and most likely represent limb position in intrinsic (postural) coordinates (Rushworth, Nixon, & Passingham, 1997; Rushworth, Johansen-Berg, &Young, 1998; Sirigu et al., 1995).
Rushworth et al. (1997) demonstrated that bilateral lesions to different regions of the monkey PPC produce doubly dissociable effects on reaching movements. Specifically, lesions to areas PG and PFG (including the lateral intraparietal region (LIP—the so-called parietal eye field) and the PRR) impair visually guided reaching in the light but do not affect reaching movements made in the dark to target positions that are defined posturally. However, the reverse is true for bilateral lesions of areas PE and PF (area 7b, area 5, and the medial intraparietal region), which severely impair reaching movements in the dark to posturally defined targets, but leave unaffected reaching movements made in the light to targets that are defined visually. These data indicate that reaching movements may be coded in extrinsic and intrinsic coordinates in different regions of the monkey PPC. Furthermore in a companion study, Rushworth and colleagues (Rushworth et al., 1998) demonstrated that while lesions to area 7b, area 5, and the medial intraparietal region do not appear to disrupt the transformation of target information from retinal coordinates into body-centred (shoulder) coordinates, they do impair the transformation between desired hand position in extrinsic coordinates and the postural configuration of the arm (intrinsic coordinates).
It remains to be clearly demonstrated whether the functional organisation of the monkey parietal lobes (investigated largely using electrophysiological recording techniques) is replicated in the human PPC (investigated primarily using neuropsychological and functional brain imaging approaches—see other papers in this volume for a discussion of this topic). And we have speculated that the bilateral organisation of neural systems coding movements in intrinsic (postural) and extrinsic (eye-centred) coordinates observed in the monkey, may be differently organised in the human PPC. Specifically, we consider that while the human right PPC may be predisposed to plan and control movements in eye-centred coordinates, the human left PPC is biased to plan and control movements in postural coordinates (note that there are strong interhemispheric connections in the undamaged human brain that would allow these two systems to interact (Gazzaniga, 2000)).
The above suggestion is consistent with the finding that optic ataxia – misreaching under visual guidance – is quite different following unilateral left and right hemisphere damage De Renzi (1996). Thus, while unilateral damage to the right PPC typically leads to so-called ‘field’ effects, in which one or both limbs misreach to targets presented in the left visual field alone, unilateral lesions of the left PPC most often produces ‘hand’ effects, where only the contralateral limb misreaches when moving to targets presented in either visual hemifield (Jackson et al., 2005, Perenin and Vighetto, 1988; Ratcliffe & Davies-Jones, 1972). It is also consistent with the finding that left PPC damage produces deficits in postural representation (Sirigu et al., 1995) whereas right PPC damage gives rise to impaired reaching movements to targets that are defined visually, but leaves unaffected reaching movements made, without vision, to targets that are defined posturally (Jackson, Newport, Husain, Harvey, & Hindle, 2000).
Irrespective of the whether the spatial representations used to guide reaching movements are more strongly lateralised in the human PPC than in the monkey, recent neuropsychological evidence clearly indicates that in humans the left superior parietal lobule at least may play a key role in actively maintaining an accurate and up-to-date representation of the current postural state of the body (Wolpert, Goodbody, & Husain, 1998). In this study we sought converging evidence for this view by using functional brain imaging techniques to study movements directed to posturally defined target locations in the absence of vision. Specifically, we used event-related functional magnetic resonance imaging (fMRI) to investigate which brain areas are specifically involved in maintaining and updating the postural (i.e., non-visual) representations of the upper limb that participate in the accurate control of reaching movements.
Section snippets
Participants
Event-related fMRI was carried out on thirteen neurologically-healthy adult volunteers (eight females; mean age 24.6 years). Twelve of the participants reported that they were right-handed and one claimed to be left-handed. Note that the BOLD activations for the left-handed subject were not qualitatively different from those observed for subjects reporting themselves to be right handed. All subjects showed a similar pattern of activation, which was visually assessed by the researchers before
Experiment 1
A key issue to investigate in this experiment was to determine whether the first movement in each set of trials, i.e., that involving a novel limb posture, would elicit increased activation, compared to movements that involved repeating a postural sequence that has been used on a previous trial or trials (e.g., the second and third movements in each set). As noted by Rushworth et al. (1998), the relation between desired hand position and an associated postural configuration is considered to be
Discussion
We used event-related functional magnetic resonance imaging (fMRI) to investigate brain areas involved in maintaining and updating postural representations of the upper limb that may participate in the accurate control of reaching movements. In Experiment 1 we investigated reaching movements made without vision from variable, posturally defined, starting positions to a fixed, posturally defined, target location (the point of the chin). In Experiment 2 we investigated reaching movements executed
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