Research reportParieto-occipital cortex and planning of reaching movements: A transcranial magnetic stimulation study
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.
Section snippets
Subjects
Fifty-six healthy volunteers (30 males and 26 females; age-range 20–53 years, mean age and standard deviation 26.9 ± 6.6 years) took part in the experiment. They were subdivided into three experimental groups, in addition to a sham and a control one. All subjects were right-handed accordingly to the Oldfield test [36] and gave written informed consent after receiving information about TMS and its related risks, in accordance with the Declaration of Helsinki. The safety guidelines for TMS were
Results
Statistical analysis showed that TMS had different effects in different scalp locations, in relation to the different timing of TMS delivery and also in relation to the presentation of targets in the central or in the peripheral visual field.
Statistical analyses have been conducted merging the results from the left and right target locations in the “peripheral condition”. This enabled to highlight potential eccentricity effects, as suggested by deficits like optic ataxia, where impairment in
Discussion
The available literature suggests the existence of a discrete dorso-medial stream involved in the planning of reaching movements, although uncertainty on causality-timing activation of these regions in humans during planning of reaching movements still exists.
The present findings show that visuomotor processing involves specific sub-regions of parieto-occipital cortex, probably with a posterior to anterior time of involvement. More posterior regions seems to be involved in central as in
Acknowledgements
The authors wish to thank Dr. Luca Weis for assistance in MR acquisitions and analysis, and Dr. Luigi Stebel for assistance in software and hardware management. This work was supported by grants from Ministero dell’Università e della Ricerca, Italy.
References (57)
- et al.
Transcranial magnetic stimulation: neurophysiological applications and safety
Brain Cogn
(2002) - et al.
Visuomotor deficits and fast recovery after area V6A lesion in monkey
Behav Brain Res
(2003) - et al.
Visuomotor transformations: early cortical mechanisms of reaching
Curr Opin Neurobiol
(1998) - et al.
Posterior parietal cortex encodes autonomously selected motor plans
Neuron
(2007) - et al.
Disordered sensorimotor transformations for reaching following posterior cortical lesions
Neuropsychologia
(2001) - et al.
Parallel direction and extent specification of planar reaching arm movements in humans
Neuropsychologia
(1996) - et al.
Separate visual pathways for perception and action
Trends Neurosci
(1992) - et al.
A general deficit of the “automatic pilot” with posterior parietal cortex lesion?
Neuropsychologia
(2006) - et al.
EEG dynamics of the frontoparietal network during reaching preparation in humans
Neuroimage
(2007) - et al.
Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping
Neuroimage
(2004)
The assessment and analyisis of handedness: the Edinburgh inventory
Neuropsychologia
Two cortical systems for reaching in central and peripheral vision
Neuron
New light through old windows: moving beyond the “virtual lesion” approach to transcranial magnetic stimulation
Neuroimage
Intention-related activity in the posterior parietal cortex: a review
Vision Res
fMRI of peripheral visual field representation
Clin Neurophysiol
Electric field of two commercial figure-8 coils in tms: calculation of focality and efficiency
Clin Neurophysiol
Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the international workshop on the safety of repetitive transcranial stimulation, June 5–7, 1996
Electroencephalogr Clin Neurophysiol
The parietal reach region codes the next planned movement in a sequential reach task
J Neurophysiol
Reach plans in eye-centered coordinates
Science
Early motor influences on visuomotor transformations for reaching: a positive image of optic ataxia
Exp Brain Res
Early coding of reaching in the parieto-occipital cortex
J Neurophysiol
Effect of lesions to area v6a in monkeys
Exp Brain Res
Direct visuomotor transformations for reaching
Nature
FMRI evidence for a ‘parietal reach region’ in the human brain
Exp Brain Res
Two periods of processing in the (circum)striate visual cortex as revealed by transcranial magnetic stimulation
Neuropsychologia
Human parietal cortex in action
Curr Opin Neurobiol
Role of the posterior parietal cortex in updating reaching movements to a visual target
Nat Neurosci
Arm-reaching neurons in the parietal area V6A of the macaque monkey
Eur J Neurosci
Cited by (17)
The neural response is heightened when watching a person approaching compared to walking away: Evidence for dynamic social neuroscience
2022, NeuropsychologiaCitation Excerpt :In the present study design, the movement of the model did not imply the use of any object or any explicit goal-directed behaviour towards the subject, thus our results suggest that even in the absence of an object or an explicit intention of an interaction, alpha and beta oscillations over parietal-occipital areas are selectively modulated by the proximity of others. As previously shown by a large body of evidence, the parietal-occipital cortex is part of the action observation network involved in the representation of space for action (Colby and Goldberg, 1999; Husain and Nachev, 2007), in motor planning (Andersen et al., 1997; Andersen and Cui, 2009; Buneo and Andersen, 2006; Busan et al., 2009), in the action observation of object and non-object directed actions (Iacoboni et al., 2004; Evangeliou et al., 2009; Buccino et al., 2001) and in processing social information during action observation (Tunik et al., 2007; Pobric and Hamilton, 2006). The present data furthermore suggest that when the model is far away, an increase of power occurs both in the alpha and in the beta bands, suggesting a reverse oscillatory pattern compared to when the model is near to the observer.
The role of the right posterior parietal cortex in prism adaptation and its aftereffects
2021, NeuropsychologiaCitation Excerpt :As to the possible role of V1 in the planning and learning of visuo-motor tasks, such as reaching a visual target, as in PA paradigms, or visuomotor coordination, in one study (Antal et al., 2004) the modulation of V1 activity by means of anodal or cathodal tDCS did not affect the performance of healthy participants in a visuomotor tracking task involving hand movements, while cathodal stimulation of extra-striate area MT+/V5 improved the participants’ performance. Conversely, single pulse TMS to the left PPC facilitated reaching movements when TMS was delivered on the parietal cortex at about half of the time from the sight of the target to hand movement, independently of target location in space (Busan et al., 2009a, see also Busan et al., 2009c, for a similar facilitatory effect for stimulation of the left dominant anterior occipital lobe and the parieto-occipital cortex). Some contribution of the hemisphere ipsilateral to the dominant hand is suggested by the finding that single pulse TMS over the parieto-occipital cortex increased reaction times in the task of reaching visual targets by the dominant right hand (Busan et al., 2009b).
Contribution of transcranial magnetic stimulation in assessing parietofrontal connectivity during gesture production in healthy individuals and brain-injured patients
2019, Neurophysiologie CliniqueCitation Excerpt :Although there are fewer virtual lesion studies of the pIPS and the SPOC than of the aIPS, the research has revealed these areas’ influence on the planning of reaching movements in humans [21,22,73]. In addition, Busan et al. evidenced, by modulating the pIPS, the SPOC and the dPM cortex during the planning of reaching movements, that visuomotor information is probably processed in parallel in these regions of interest [5,6]. At rest, the connections between the pIPS and the SPOC and between the dPM cortex and M1 (as evidenced by ppTMS protocols) differ from those observed for the dorsolateral network.
Human parietal and primary motor cortical interactions are selectively modulated during the transport and grip formation of goal-directed hand actions
2013, NeuropsychologiaCitation Excerpt :It has been suggested that human SPOC may be the human homologue of monkey V6A (Connolly et al., 2003), an area with reach-selective properties (Fattori et al., 2001, 2005; Galletti, Kutz, Gamberini, Breveglieri, & Fattori, 2003). More compellingly, both event-related TMS over SPOC in healthy individuals (Busan, Barbera, et al., 2009; Busan, Monti, et al., 2009; Vesia et al., 2010) and optic ataxia patients with parietal damage (Himmelbach et al., 2009; Karnath & Perenin, 2005; Perenin & Vighetto, 1988) highlight the critical role of SPOC in reach, a view largely compatible with the present data. Collectively, these findings support the idea that SPOC may be critical in relaying extrinsic properties like target spatial information (Vesia et al., 2010) to ipsilateral M1.
Brain metabolite concentrations across cortical regions in healthy adults
2011, Brain ResearchCitation Excerpt :ACC plays a role in cognitive functions such as reward anticipation, decision making, empathy, and emotion (Phillips et al., 2003; Walton et al., 2007; Walton and Mars, 2007). Parieto–occipital cortex (POC) is a central node in the dorsomedial visual stream, and is thought to be responsible for integration of visual information necessary for behaviors such as reaching and grasping (Chapman et al., 2002; Busan et al., 2009). The two regions are anatomically and functionally connected as part of the default mode network (Gusnard and Raichle, 2001).