Elsevier

Neuroscience

Volume 223, 25 October 2012, Pages 258-268
Neuroscience

Integration of visual and proprioceptive afferents in kinesthesia

https://doi.org/10.1016/j.neuroscience.2012.07.059Get rights and content

Abstract

Proprioceptive signals are of prime importance in kinesthesia. However, in conditions of visuo-proprioceptive conflicts, strong visual-evoked biases can be observed. In three experiments, we parsed the interaction between visual and proprioceptive afferents using the ‘mirror box’ paradigm. Participants’ left arm, the image of which was reflected in a mirror, was passively moved into flexion/extension or remained static. In Experiment 1 proprioceptive afferents of the unseen static right arm were masked with diffuse arm vibration. In Experiments 2 and 3, afferent signals were enhanced by muscle vibration of biceps or triceps stretch receptors. Illusory arm movements were evaluated with subjective reports and matching adjustments. Results revealed that participants did not experience kinesthetic illusions when the mirror reflected the image of a static arm while proprioceptive afferents conveyed signals of a moving arm (Experiment 2). In this specific case, vision apparently contributed much more strongly to the final percept than proprioceptive signals. However, in most circumstances, the percept reflected integration of both afferent signals (Experiments 1–3). For instance, when both sensory channels conveyed signals of arm displacement but in the opposite direction, kinesthetic illusions occurred but were either proprioceptively (vibration illusion) or visually driven (mirror illusion), according to individual sensorial preferences (Experiments 2 and 3). These results indicate that kinesthesia is the product of cooperative integration processes in which the final percept strongly depends on the experimental conditions as well as sensorial preferences. The observed changes in the relative contribution of each input across experimental conditions likely reflect reliability-dependent weights.

Highlights

► We examined visual and proprioceptive integration in the mirror box paradigm. ► Reflection of a static limb through a mirror abolishes vibration-evoked illusion. ► The relative weight of visual and proprioceptive channels is context-dependent. ► Kinesthetic illusion in bimodal condition can be predicted from unimodal conditions.

Introduction

Kinesthesia refers to the sense of position and movement of our limbs and trunk. Among proprioceptive afferents, the principal muscle receptor involved in kinesthesia is the muscle spindle that has been widely investigated by the use of vibration. Specifically, vibration, applied to a muscle–tendon, activates mainly the primary spindle endings (Ia fibers), for which the firing rate seems to be interpreted by the CNS as an elongation of that muscle (Burke et al., 1976, Roll et al., 1989, Roll et al., 2009). When vibration is applied on one particular muscle, the erroneous interpretation induces motor effects (Eklund, 1972, Goodwin et al., 1972, Roll and Roll, 1988, Romaiguere et al., 1991, Caudron et al., 2008, Caudron et al., 2010) or illusory sensation of joint displacement also called vibratory illusion (Goodwin et al., 1972, Gilhodes et al., 1986, Ceyte et al., 2007). For instance, vibration, applied on either the biceps or triceps of an unseen static arm, induces illusion of arm displacement in the direction that would have stretched the receptor bearing muscle (Goodwin et al., 1972, Roll and Roll, 1988). In contrast, when applied to the whole body/segments (such as using a road drill) or concurrently on two antagonist muscles, vibration substantially degrades afferent proprioceptive responsiveness and therefore position perception (Ribot et al., 1986, Roll et al., 1989, Bock et al., 2007).

Although of prime importance (Teasdale et al., 1993), proprioceptive afferents interact with other senses, such as vision, in the perception of position and movement (Maravita et al., 2003). For instance, a combination of synchronous visual and touch stimuli are sufficient to mislead the nervous system into self-attribution of a rubber hand (Botvinick and Cohen, 1998, Dummer et al., 2009). In this paradigm, when stimuli were temporally but not spatially congruent, intersensory bias occurred and the felt position of one’s own hand is relocated toward the location of the rubber hand (Botvinick and Cohen, 1998, Kammers et al., 2009). Similarly, reflection of one moving hand through a mirror placed along the midline axis can give the appearance of symmetrical bimanual movements (“mirror illusion”). Such visual-evoked biases likely reflect “optimal” integration processes in which the relative weight of each sensory input is proportional to its reliability (Ernst and Bülthoff, 2004).

The purpose of our study was to parse further the interaction between visual and proprioceptive afferents in kinesthesia. Healthy participants were required to report illusory right arm displacement evoked by a combination of visual and proprioceptive manipulation. Visual afferents were manipulated through the mirror box paradigm in which participants could see the reflection of their passively moved left arm through a mirror orientated parallel to their midsagittal axis. Proprioceptive afferents on the unseen right arm were either degraded/masked through diffuse vibrotactile stimulation (Experiment 1) or enhanced by targeted muscle vibration (Experiments 2 and 3). The interaction between visual and proprioceptive signals was evaluated in uni- or bimodal stimulation conditions in which the two sensory channels conveyed either congruent (co-directional) or opposite (contra-directional) signals about arm displacement.

Section snippets

Participants

Fifteen participants (10 females, 5 males, 14 right-handed), ranging in age from 18 to 29 years (mean age = 21.2 years) participated in Experiment 1. Eleven right-handed participants (8 females, 3 males), ranging in age from 20 to 29 years (mean age 21.8 years) participated in Experiment 2, four of whom already participated in Experiment 1. One of these participants did not experience any vibratory illusion and was not further considered for the experiment. Eighteen participants (12 females, 6 males,

Subjective reports

Reflection of the passively moving left arm through the mirror-evoked illusions of right arm displacement (“mirror illusion”) in the same direction. Mirror illusion was experienced in 98% and 96% of the trials when the vibrotactile mask was present or absent, respectively. Passive displacement of the left arm evoked occasional illusions of right arm displacement in the other two visual conditions (no mirror: 35%; no vision: 31%) when the vibrotactile mask was present. When the vibrotactile mask

Mirror illusion attests of visual signal contribution to kinesthesia

When looking at the mirror reflection of their passively moved forearm in Experiments 1–3, participants most frequently reported illusory displacement of their other forearm. The occurrence and intensity of this kinesthetic illusion are particularly interesting considering that some authors did not report such an illusion in healthy subjects (Zampini et al., 2004). In these previous reports, passive displacements were performed by the experimenters themselves and when reported, displacement

Conclusion

The limited consciousness of proprioceptive afferent signals (Mon-Williams et al., 1997, Fourneret and Jeannerod, 1998) leads to large perceptual biases when visual cues, not congruent with the actual position of the body segment, are provided. Our results indicate, however, that kinesthesia is the product of cooperative integration processes in which the relative contribution of each channel to the final percept depends strongly on the experimental conditions and individual sensorial

Author contributions

M.G., S.P., R.N., S.V., A.B. and J.P.B. participated in the conception, design and conduction of the studies. All the authors participated to the interpretation of the data. The original draft was prepared by M.G. but the six authors critically revised the manuscript before approving the final version.

Acknowledgements

Pierre Alain Barraud provided expert technical assistance for the motorized manipulandum. We thank Prof. Michael Gresty for English language editing.

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