Proprio-tactile integration for kinesthetic perception: An fMRI study
Introduction
Human ability to perceive one's own body movements, whether this concerns a single segment or the whole body, is mainly based on the processing of related information from multiple sensory modalities. Central mechanisms underlying perception of one's own limb movements have been already investigated through various neuroimaging protocols using passive (Mima et al., 1999, Weiller et al., 1996) or imagined movement (Decety, 1996, Stephan et al., 1995) or vibration-induced kinesthetic illusions (Casini et al., 2006, Naito et al., 1999; Radovanovic et al., 2002, Romaiguere et al., 2003). However, it is uncertain how different sensory channels cooperate in the kinesthetic perception of a body segment. Indeed, one can assume that an imagined movement does not solicit any specific sensory channel; inversely, when a passive movement is imposed to the subject, multiple sensory messages related to the movement of his/her limb are indistinctly co-activated. It is well known that vibration-induced illusory perceptions of movement of one's own body concern mainly muscle spindle primary afferents. Vibrations applied to a muscle group give rise to a proprioceptive message that is erroneously interpreted by the CNS as an actual movement in the direction of the stretching of the vibrated muscle (Goodwin, McCloskey, & Matthews, 1972; Roll & Vedel, 1982).
The benefit of the convergence of various sensory sources for perceptual and motor purposes has been extensively studied in various approaches concerning either single (Collins, Refshauge, & Gandevia, 2000; Tardy-Gervet, Gilhodes, & Roll, 1986) or whole-body movements (Kavounoudias, Roll, & Roll, 2001; Mergner & Rosemeier, 1998; Oie, Kiemel, & Jeka, 2002). In particular, using the human upright stance model Kavounoudias et al. (2001) investigated the relative contribution of the cutaneous information from the plantar foot soles and of the proprioceptive inputs from ankle muscles in controlling postural balance. Perceptual integration resulting from visual and proprioceptive co-stimulations or from tactile and proprioceptive co-stimulations have been also reported by Tardy-Gervet et al. (1986) and Lackner and Levine (1979), respectively. All these studies show that co-processing of various convergent inputs is crucial to properly assess the body configuration and its changes.
However, how and where the multisensory inputs are integrated by the CNS is not yet fully elucidated. In particular, it is debated whether specific cerebral substrates are devoted to such integrative processing (Calvert & Thesen, 2004; Soto-Faraco, Kingstone, & Spence, 2003). Nowadays, two main hypotheses compete about the mechanisms mediating multisensory integration: one states that multisensory integration might involve heteromodal brain areas on which different sensory information arising from different unimodal areas would converge. This hypothesis is supported by clinical data showing that focal lesions in the right parietal cortex can result in multisensory deficits (Galati et al., 2000). In addition, heteromodal neurons sensitive to different stimuli were found in the superior colliculi of the cat (Stein, Meredith, & Wallace, 1993; Wallace, Meredith, & Stein, 1992) and also in the premotor and parietal areas of the monkey (Graziano & Gross, 1998; Grefkes & Fink, 2005). These neurons, which responded in a supra-additive manner when spatially congruent stimuli from different origins were simultaneously presented to the animal, could be considered good candidates for integrative processing. Moreover, results from neuroimaging studies focusing on the crossmodal binding in attention or recognition tasks have shown that heteromodal brain regions are specifically activated in presence of different sensory inputs (Bremmer, Schlack, Shah et al., 2001; Calvert, Campbell, & Brammer, 2000; Calvert & Thesen, 2004; Downar, Crawley, Mikulis, & Davis, 2000; Macaluso & Driver, 2001). Together, these data support the idea that specific cerebral sites and networks subserve multisensory integrative mechanisms.
However, this hierarchical model is challenged by another based on a more parallel organization (Bushara, Grafman, & Hallett, 2001; Ettlinger & Wilson, 1990; Hadjikhani & Roland, 1998; Olson, Gatenby, & Gore, 2002). Indeed, the “communication relay model” recently proposed by Olson et al. (2002) states that specific heteromodal sites are not required for integrative processing and that what is crucial for the CNS is to detect the temporal coincidence of various sensory signals related to the same event. In line with the assumption of Hadjikhani and Roland (1998), Olson et al. (2002) propose that a subcortical relay for the different parallel sensory pathways would be responsible for the detection of such a temporal coherence.
To go further into how multisensory cues are co-processed by the CNS for movement perception, we designed an experiment in which tactile and/or proprioceptive stimulations induced well-oriented illusory perceptions of hand movement. For this, wrist tendon vibration and/or moving tactile stimulation was applied to and under the hand of the participants. First we investigated whether the same cerebral network was activated during the illusory perception of a hand rotation induced by the proprioceptive or the tactile stimulation. Second, by co-stimulating synchronously these two sensory channels, we investigated whether heteromodal structures were specifically activated in the co-stimulation condition.
Section snippets
Participants
Ten right-handed volunteers (eight women and two men; mean age 31.5 ± 10.7 years) with no history of neurological disease gave informed consent to participate in this study as required by the Helsinki declaration. The experiment was approved by the local Ethics Committee (CCPPRB Marseille 1 #04/41). The inclusive criteria of the study were the classical recommendations relative to the fMRI environment.
Experimental device
As shown in Fig. 1, the tactile stimulation device consisted of a rotatory disk (40 cm diameter, 7
Characteristics of the kinesthetic hand illusions induced by a tactile and/or a proprioceptive stimulation (Fig. 2)
For all the subjects tested, the tactile and proprioceptive stimulations delivered separately or conjointly always gave rise to a powerful illusion of rotation of the subject's right hand in a clockwise direction. As expected, the direction of the hand movement illusions was identical in unimodal and bimodal conditions. However, the cinematic parameters of the movement varied according to the sensory stimulation conditions: illusions occurred earlier and were stronger when the subjects’ hand
Cortical areas
Results show that regardless of the sensory modality, the same large-scale network of sensorimotor brain areas was predominantly activated during the movement illusions of the subjects’ right hand. Activations were found in the motor and premotor cortices, the supplementary motor area, the inferior parietal lobule, the cingulate motor areas, and the cerebellum. These brain regions were those previously evidenced by various groups during vibration-induced illusory movements (Casini et al., 2006,
Acknowledgments
This research was supported by grants from CNES (Centre National d’Etudes Spatiales) and OPPBTP (Organisme Professionnel de Prévention du Bâtiment et des Travaux Publics).
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