Information processing in human parieto-frontal circuits during goal-directed bimanual movements
Introduction
Single unit and lesion studies in the macaque have revealed how parieto-precentral circuits can generate spatial representations from sensory information during goal-directed actions (Rizzolatti et al., 1998, Johnson et al., 1996, Wise et al., 1997, Rushworth et al., 1997). Furthermore, it has been shown that different sensory modalities are processed within distinct parieto-frontal circuits (Rizzolatti et al., 1998, Johnson et al., 1996, Burnod et al., 1999) (Fig. 3A). More specifically, anterior parietal areas PE and PEip respond to somatosensory stimuli (Iwamura and Tanaka, 1996, Lacquaniti et al., 1995, Johnson et al., 1996) and project to posterior precentral cortex [medio-caudal portion of area F2] (Johnson et al., 1996, Rizzolatti et al., 1998, Fogassi et al., 1999, Lacquaniti et al., 1995, Marconi et al., 2001). Posterior parietal areas MIP, PEc, and V6A respond additionally to visual stimuli (Battaglia-Mayer et al., 2001, Galletti et al., 2001, Johnson et al., 1996, Colby and Duhamel, 1991, Galletti et al., 2003, Breveglieri et al., 2002) and project to anterior precentral cortex [rostro-lateral portion of F2] (Matelli et al., 1998, Rizzolatti et al., 1998, Marconi et al., 2001, Johnson et al., 1996, Fogassi et al., 1999). Despite growing evidence supporting a close functional correspondence in the organization of parietal and frontal cortex of macaques and humans (Bremmer et al., 2001, Passingham, 1998, Sereno et al., 2001, Toni et al., 2001b), to date, there has been no empirical support for a similar modality-specific segregation of the human parieto-frontal circuitry in the context of goal-directed movements. A few imaging studies have explored this issue by using simple pointing paradigms (Ellermann et al., 1998, Inoue et al., 1998, Lacquaniti et al., 1997, Connolly et al., 2000), but provided no evidence for spatially independent sensorimotor processing streams in the parieto-frontal system. However, the scope of these negative results might be limited to the experimental setting of these studies, since the semi-ballistic nature of simple pointing paradigms appears inadequate for evoking on-line sensory guidance of movement in space.
Here, we aim at understanding the specific contributions of superior parietal and dorsal precentral cortex to sensorimotor processing. Building on the known functional organization of parieto-frontal circuits in macaques, we have tested the hypothesis that in humans, as in macaques, performance of movements guided by somatosensory information engages anterior parietal and posterior precentral regions. Conversely, movements performed with both visual and somatosensory information should additionally activate posterior parietal and anterior precentral areas. To ensure that sensory information was actually used for on-line guidance of movements, rather than for planning semi-ballistic movements, we have exploited the behavioral phenomenon of directional interference. Directional interference emerges when two limbs are moved simultaneously along directionally incompatible trajectories, as when one tries to concurrently draw a vertical line with the left arm and a horizontal line with the right arm. Under these circumstances, a mutual bias of movement directions automatically emerges between the limbs movements (Swinnen et al., 2001). Consequently, moving along incompatible directions requires subjects to permanently monitor the limbs' positions in space to prevent limb trajectories from becoming substantially biased. Here, we induced directional interference by using combinations of cyclical, metronome-paced ‘line-drawing’ movements (i.e., moving along a vertical line at all times) and ‘star-drawing’ movements (i.e., moving along systematically varying orientations deviating either +45, 90 or −45° from the vertical—see Fig. 1). We applied functional magnetic resonance imaging (fMRI) while subjects performed either the directionally compatible StarStar task (i.e., symmetrical star-drawing with the left and the right hand) or the directionally incompatible LineStar/StarLine tasks (i.e., line-drawing with one hand while star-drawing with the other hand). These tasks were performed either under somatosensory guidance only or with additional visual information. Continuous kinematic measurements obtained during task performance in the scanner confirmed that the presence of visual information does not substantially alter the behavioral effects of directional interference (Puttemans et al., 2004). This singular feature of directional interference tasks makes it possible to vary the amount and type of sensory information used during movement performance without affecting motor output. Therefore, we have exploited directional interference to drive subjects to rely on sensory guidance of movements, while manipulating the type of sensory information available for on-line control of motor performance. By combining this robust psychophysical protocol with fMRI, we have been able to isolate modality-specific brain responses during on-line guidance of goal-directed movements, other factors being equal.
Section snippets
Subjects
Eleven volunteers (6 females, 5 males, aged 22 ± 2 (S.D.) years) participated in the experiment. All were right-handed (Oldfield, 1971), naïve with respect to the task and had normal vision. None of them participated in regular musical training. All subjects gave written informed consent before participating in the experiment which was approved by the local ethical committee of K.U.Leuven. Subjects were paid for their services.
Experimental setup
Subjects lay supine in the scanner with their upper arms next to the
Behavioral data
Directional interference was quantified by mean orientation error (αError) and orientation variability (αSD), averaged between wrists. Both αError and αSD were significantly increased during the execution of the directionally incompatible (StarLine/LineStar) as compared to the directionally compatible tasks (StarStar) (F1,10 > 9.3, P < 0.05; Figs. 2A, B). During the incompatible tasks, interference was particularly high when subjects had to trace non-parallel orientations, reaching the highest
Discussion
We have manipulated the availability of visual information during performance of a bimanual directional interference task in order to assess the spatial segregation of modality-specific neural activity in the human parieto-frontal circuitry. The behavioral results confirm that the inter-limb bias in the execution of different movement directions (directional interference) is indifferent to the presence of visual information. However, the imaging results indicate that visual information strongly
Conclusions
We have characterized the spatial distribution and inter-regional couplings of modality-specific responses in the human superior parietal and dorsal precentral cortex during the integration of sensory information to guide goal-directed movements. We confirmed that in humans, as in macaques, performance of movements guided by somatosensory information engages anterior parietal and posterior precentral regions, while movements performed with both visual and somatosensory feedback activate
Acknowledgments
This study was supported by the Flanders Fund for Scientific Research (FWO Project- G.0460.04) and the Research Fund K.U.Leuven (OT/03/61).
References (85)
- et al.
Hierarchical processing of tactile shape in the human brain
Neuron
(2001) - et al.
Polymodal motion processing in posterior parietal and premotor cortex: a human fMRI study strongly implies equivalencies between humans and monkeys
Neuron
(2001) - et al.
Heterogeneity of extrastriate visual areas and multiple parietal areas in the macaque monkey
Neuropsychologia
(1991) - et al.
Brain activation related to the representations of external space and body scheme in visuomotor control
NeuroImage
(2001) - et al.
Brain activation related to the representations of external space and body scheme in visuomotor control
NeuroImage
(2001) - et al.
Activation of visuomotor systems during visually guided movements: a functional MRI study
J. Magn. Reson.
(1998) - et al.
Analysis of fMRI time-series revisited
NeuroImage
(1995) - et al.
Psychophysiological and modulatory interactions in neuroimaging
NeuroImage
(1997) - et al.
Representation of reaching and grasping in the monkey postcentral gyrus
Neurosci. Lett.
(1996) - et al.
Processing of tactile and kinesthetic signals from bilateral sides of the body in the postcentral gyrus of awake monkeys
Behav. Brain Res.
(2002)
Visuomotor transformations for reaching to memorized targets: a PET study
NeuroImage
Spatial attention and crossmodal interactions between vision and touch
Neuropsychologia
Multimodal spatial representations engaged in human parietal cortex during both saccadic and manual spatial orienting
Curr. Biol.
Parietofrontal circuits for action and space perception in the macaque monkey
NeuroImage
Imaging the premotor areas
Curr. Opin. Neurobiol.
The organization of the cortical motor system: new concepts
Electroencephalogr. Clin. Neurophysiol.
The left hemisphere and the selection of learned actions
Neuropsychologia
Cerebral dominance for action in the human brain: the selection of actions
Neuropsychologia
Topographical layout of hand, eye, calculation, and language-related areas in the human parietal lobe
Neuron
Intention-related activity in the posterior parietal cortex: a review
Vision Res.
Constraints during bimanual coordination: the role of direction in relation to amplitude and force requirements
Behav. Brain Res.
Movement preparation and motor intention
NeuroImage
Windows on the brain: the emerging role of atlases and databases in neuroscience
Curr. Opin. Neurobiol.
Eye–hand coordination during reaching: II. An analysis of the relationships between visuomanual signals in parietal cortex and parieto-frontal association projections
Cereb. Cortex
Somatosensory cells in the parieto-occipital area V6A of the macaque
NeuroReport
Direct visuomotor transformations for reaching
Nature
Parieto-frontal coding of reaching: an integrated framework
Exp. Brain Res.
Visual feedback reduces bimanual coupling of movement amplitudes, but not of directions
Exp. Brain Res.
Processing visual feedback information for movement control
J. Exp. Psychol. Hum. Percept. Perform.
A common reference frame for movement plans in the posterior parietal cortex
Nat. Rev., Neurosci.
Space and attention in parietal cortex
Annu. Rev. Neurosci.
Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: a dual tracer study
J. Comp. Neurol.
A comparison of frontoparietal fMRI activation during anti-saccades and anti-pointing
J. Neurophysiol.
fMRI evidence for a ‘parietal reach region’ in the human brain
Exp. Brain Res.
A quantitative analysis of responses of direction-sensitive neurons in somatosensory cortex of awake monkeys
J. Neurophysiol.
Characterization of the human visual V6 complex by functional magnetic resonance imaging
Eur. J. Neurosci.
Role of the posterior parietal cortex in updating reaching movements to a visual target
Nat. Neurosci.
Functional anatomy of nonvisual feedback loops during reaching: a positron emission tomography study
J. Neurosci.
The Human Brain: Surface, Blood Supply, and Three-Dimensional Sectional Anatomy
The utilization of visual feedback information during rapid pointing movements
Q. J. Exp. Psychol., A
Visual responses in the dorsal premotor area F2 of the macaque monkey
Exp. Brain Res.
Spatial registration and normalization of images
Hum. Brain Mapp.
Cited by (47)
Neurophysiological Correlates of Adaptation and Interference during Asymmetrical Bimanual Movements
2020, NeuroscienceCitation Excerpt :Studies in non-human primates have shown that the corpus callosum allows for hand-specific information to be projected between the hemispheres, particularly from the supplementary motor area (SMA) and pre-SMA (Liu et al., 2001). Evidence from imaging studies in humans demonstrates increased activity of homologous areas in each hemisphere during interference caused by directional stimuli, particularly in the parietal-premotor network (Wenderoth et al., 2004, 2005, 2006). Additionally, interference is reduced in callosotomy patients, who can accurately perform asymmetrical drawing and force production tasks, presumably due to diminished neural crosstalk (Franz et al., 1996; Diedrichsen et al., 2003).
Cerebellar gray matter explains bimanual coordination performance in children and older adults
2018, Neurobiology of AgingCitation Excerpt :In addition, this cerebellar region (lobule VI) was the best predictor of performance in children, suggesting that the maturation of accurate predictive estimates, which have been associated with Purkinje cell activity in the cerebellar vermis (Laurens et al., 2013), drives bimanual coordination performance in this population. This result is consistent with previous findings showing that lobule VI is critical for motor tasks (i.e., sequence learning and visuomotor adaptation) and especially for spatial tasks (including interlimb coordination tasks (Beets et al., 2015; Debaere et al., 2003, 2004a,b; Goble et al., 2010; Santos Monteiro et al., 2017; Wenderoth et al., 2004, 2006). This result also supports previous findings based on smooth pursuit eye movements and split-belt walking, suggesting that the maturation of motor functions is determined by the developmental state of the cerebellum (Ego et al., 2016; Vasudevan et al., 2011).
fMRI characterisation of widespread brain networks relevant for behavioural variability in fine hand motor control with and without visual feedback
2017, NeuroImageCitation Excerpt :This finding is supported by both human and primate studies demonstrating that the parietal cortex and its projections to the dorsal and ventral premotor cortex are fundamental to visuomotor processing (Calton et al., 2002; Desmurget et al., 1999; Ellermann et al., 1998; Goodale and Milner, 1992; Hamzei et al., 2002; Jeannerod et al., 1995; Tanne-Gariepy et al., 2002) and particularly in the reactive control of fine-tuned precision grip tasks (Dafotakis et al., 2008; Davare et al., 2007; Ehrsson et al., 2001; Haller et al., 2009). The co-operation of these areas in transforming visual information into action occurs via the strong connections between them which form parallel parieto-premotor circuits (Rizzolatti et al., 1998; Wenderoth et al., 2006; Wise et al., 1997). The IPL in particular has been shown to help control movements by working as an interface between the perceptual and motor systems (Grefkes and Fink, 2005).
Automatic online control of motor adjustments in reaching and grasping
2014, Neuropsychologia