Parieto-occipital cortex and planning of reaching movements: A transcranial magnetic stimulation study

Abstract

A large amount of evidence supports a role for the parietal and frontal cortex in the planning of reaching movements. Nevertheless, neither the timing of involvement of these areas nor if and how their activity can be influenced by external stimuli has been clarified. The parieto-occipital cortex has been investigated by applying transcranial magnetic stimulation (TMS) at 25% (Time 1), 50% (Time 2) and 75% (Time 3) of the reaction time from a go signal to hand movement. No local effect was found with Time 1, since pulses were administered before subjects opened their eyes. Reduction of reaction time was observed at Time 2 when stimuli were applied over the anterior occipital lobe, parieto-occipital cortex and posterior parietal cortex. The effect on the posterior parietal cortex reverted when Time 3 was used. The present data confirm the existence, in humans, of a dorso-medial set of areas involved in on-line planning of reaching movements. Moreover, they provide novel evidence on the time course of this involvement. Finally, present data show that it is possible to interact with the flow of activity along this stream by appropriately delivering TMS pulses.

Introduction

Two different pathways for visual information processing are well established, namely a ventral and a dorsal one. The former participates in constructing the representation of the world by identifying objects and events, attaching meaning and significance to them, and establishing their causal relations. The dorsal stream plays a critical role in real-time control of action by transforming the information about the location of objects into the coordinate frames of the effectors performing the action [23], [31]. Evidence suggests that, within the dorsal stream, a dorsomedial pathway is mainly involved in the production of reaching related movements and in controlling “on-line” actions, and a dorsolateral stream is involved in both reaching and grasping movements and in space perception [22], [40]. However, an overlapping between the two pathways has been suggested [40].

The temporal aspect of planning reaching movements in the dorsal stream has also been investigated. A serial hierarchy of analytic steps exists [18], but the central nervous system is organized into densely interconnected populations of neurons and parallel processing of visuo-spatial information has been more appropriately proposed [27], [28]. It has been suggested that the transformation of visuomotor coordinates takes place at the same time in a set of widely distributed cortical areas [9] and different activations within parieto-frontal circuits may take place concurrently [4], [22]. Recently, an electroencephalography study described the dynamics of the parieto-frontal activation during the preparation of a simple reaching movement [33]. The parietal and frontal areas showed two simultaneous activations at about 100 ms intervals, well before the onset of the movement. Accordingly, several studies [16], [20], [21] have already shown that neurons in the posterior parietal cortex become active well before the appearance of any electromyographic movement-related activity, thus confirming the role played by these areas in the planning of reaching [2], [5], [8], [10], [12], [17], [48], [49]. Finally, recent studies in monkeys showed the onset of misreaching after the creation of very selective lesions involving the most posterior part of the superior parietal lobule [6], [7]. Those observations have been extended in both healthy humans [39] and in patients with selected parietal lesions [27], [30].

In this context, transcranial magnetic stimulation (TMS) has largely been used in different studies to investigate the relationship between the parietal cortex and visuomotor processing [13] in healthy humans. TMS is a non-invasive technique that, by inducing an electrical field, inhibits or facilitates information processing in stimulated brain areas during execution of a task [1], [46], [47]. Apart from studies on attention and/or eye movements [32], [41], [52], TMS was applied over the posterior parietal cortex during reaching movements, and showed that subjects were unable to correct the ongoing movement following a jump of the target [15]. The possibility to interfere with early stages of spatial processing after TMS of the posterior parietal cortex has been demonstrated in a study on memory-delayed reaching movements [55]. In spite of the available data, however, uncertainty on causality-timing activation of these regions in humans during planning of reaching movements still exists.

Starting from this evidence, in the present study we investigated the role of the parieto-occipital cortex by assessing its involvement in the planning of reaching movements in humans during different time windows and with respect to different target locations in space. In particular, we evaluated the effects of TMS on closely spaced regions of the cortex and on central vs. peripheral target position during planning of reaching movements. We hypothesized that TMS might intervene with different effects in relation to the point of stimulation, and in relation to central and peripheral vision of target location during definite time-windows of stimulation. The results confirmed this hypothesis, supporting the existence of a discrete dorso-medial stream for the processing of visuomotor information. Along this stream, more posterior regions seem to be concerned with both central and peripheral vision, while in more anterior regions a preference for centrally located targets was found.