Abstract
Reaching movements are rapidly adapted following training with rotated visual feedback of the hand (motor recalibration). Our laboratory has also found that visuomotor adaptation results in changes in estimates of felt hand position (proprioceptive recalibration) in the direction of the visuomotor distortion (Cressman and Henriques 2009, 2010; Cressman et al. 2010). In the present study, we included an additional method for measuring hand proprioception [specifically, proprioceptive-guided reaches of the unadapted (left) hand to the robot-guided adapted (right) hand-target] and compared this with our original perceptual task (estimating the felt hand position of the adapted hand relative to visual reference markers/the body midline), as well as to no-cursor reaches with the adapted hand (reaching to visual and midline-targets), to better identify whether changes in reaching following adaptation to a 50° rightward-rotated cursor reflect sensory or motor processes. Results for the proprioceptive estimation task were consistent with previous findings; subjects felt their hand to be aligned with a reference marker when it was shifted approximately 4° more in the direction of the visuomotor distortion following adaptation compared with baseline conditions. Moreover, we found similar changes in the proprioceptive-guided reaching task such that subjects misreached 5° in the direction of the cursor rotation. However, these results were true only for proprioceptive-guided reaches to the adapted hand, as reaches to the body midline were not affected by adaptation. This suggests that proprioceptive recalibration is restricted to the adapted hand and does not generalize to the rest of the body; this truly reflects a change in the sensory representation of the hand rather than changes in the motor program. This is in contrast to no-cursor reaches made with the adapted hand, which show reach after-effects for both visual targets and the midline, suggesting that reaches with the adapted hand reflect more of a change in the motor system. Our results also shed light on previous studies that may have misattributed these sensory and motor changes.
Similar content being viewed by others
References
Bernier P, Gauthier GM, Blouin J (2007) Evidence for distinct, differentially adaptable sensorimotor transformations for reaches to visual and proprioceptive targets. J Neurophysiol 98:1815–1819
Berniker M, Kording K (2008) Estimating the sources of motor errors for adaptation and generalization. Nat Neurosci 11:1454–1461
Clower DM, Boussaoud D (2000) Selective use of perceptual recalibration versus visuomotor skill acquisition. J Neurophysiol 84:2703–2708
Craske B, Gregg SJ (1966) Prism after-effects: identical results for visual targets and unexposed limb. Nature 212:104–105
Cressman EK, Henriques DYP (2009) Sensory recalibration of hand position following visuomotor adaptation. J Neurophysiol 102:3505–3518
Cressman EK, Henriques DYP (2010) Reach adaptation and proprioceptive recalibration following exposure to misaligned sensory input. J Neurophysiol 103:1888–1895
Cressman EK, Salomonczyk D, Henriques DYP (2010) Visuomotor adaptation and proprioceptive recalibration in older adults. Exp Brain Res 205:533–544
Djikerman HC, de Haan EH (2007) Somatosensory processes subserving perception and action. Behav Brain Sci 30:189–201
Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15(1):20–25
Harris CS (1963) Adaptation to displaced vision: visual, motor, or proprioceptive change? Science 140:812–813
Harris CS (1965) Perceptual adaptation to inverted, reversed, and displaced vision. Psychol Rev 72:419–444
Hay JC, Pick HL Jr (1966) Visual and proprioceptive adaptation to optical displacement of the visual stimulus. J Exp Psychol 71:150–158
Held R, Bauer JA Jr (1974) Development of sensorially-guided reaching in infant monkeys. Brain Res 71:265–271
Henriques DYP, Soechting JF (2003) Bias and sensitivity in the haptic perception of geometry. Exp Brain Res 150:95–108
Izawa J, Criscimagna-Hemminger SE, Shadmehr R (2012) Cerebellar contributions to reach adaptation and learning sensory consequences of action. J Neurosci 32:4230–4239
Jones SAH, Cressman EK, Henriques DYP (2010) Proprioceptive localization of the left and right hands. Exp Brain Res 204:373–383
Jones SAH, Fiehler K, Henriques DYP (2012) A task-dependent effect of memory and hand-target on proprioceptive localization. Neuropsychologia 50:1462–1470
Kesten H (1958) Accelerated stochastic approximation. Ann Math Stat 29:41–59
Ostry DJ, Darainy M, Mattar AA, Wong J, Gribble PL (2010) Somatosensory plasticity and motor learning. J Neurosci 30:5384–5393
Redding GM, Wallace B (1978) Sources of “overadditivity” in prism adaptation. Percept Psychophys 24:58–62
Redding GM, Wallace B (1988) Adaptive mechanisms in perceptual-motor coordination: components of prism adaptation. J Mot Behav 20:242–254
Redding GM, Wallace B (1996) Adaptive spatial alignment and strategic perceptual-motor control. J Exp Psychol Hum Percept Perform 22:379–394
Redding GM, Wallace B (1997) Prism adaptation during target pointing from visible and nonvisible starting locations. J Mot Behav 29:119–130
Redding GM, Wallace B (2001) Calibration and alignment are separable: evidence from prism adaptation. J Mot Behav 33:401–412
Redding GM, Wallace B (2002) Strategic calibration and spatial alignment: a model from prism adaptation. J Mot Behav 34:126–138
Redding GM, Wallace B (2003) Dual prism adaptation: calibration or alignment? J Mot Behav 35:399–408
Redding GM, Wallace B (2006) Generalization of prism adaptation. J Exp Psychol Hum Percept Perform 32:1006–1022
Redding GM, Rossetti Y, Wallace B (2005) Applications of prism adaptation: a tutorial in theory and method. Neurosci Biobehav Rev 29:431–444
Salomonczyk D, Cressman EK, Henriques DY (2011) Proprioceptive recalibration following prolonged training and increasing distortions in visuomotor adaptation. Neuropsychologia 49:3053–3062
Salomonczyk D, Henriques DY, Cressman EK (2012) Proprioceptive recalibration in the right and left hands following abrupt visuomotor adaptation. Exp Brain Res 217:187–196
Simani MC, McGuire LM, Sabes PN (2007) Visual-shift adaptation is composed of separable sensory and task-dependent effects. J Neurophysiol 98:2827–2841
Synofzik M, Thier P, Lindner A (2006) Internalizing agency of self-action: perception of one’s own hand movements depends on an adaptable prediction about the sensory action outcome. J Neurophysiol 96:1592–1601
Synofzik M, Lindner A, Thier P (2008) The cerebellum updates predictions about the visual consequences of one’s behavior. Curr Biol 18:814–818
Templeton WB, Howard IP, Wilkinson DA (1974) Additivity of components of prismatic adaptation. Percept Psychophys 15:249–257
Treutwein B (1995) Adaptive psychophysical procedures. Vision Res 35:2503–2522
van Beers RJ, Wolpert DM, Haggard P (2002) When feeling is more important than seeing in sensorimotor adaptation. Curr Biol 12:834–837
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Clayton, H.A., Cressman, E.K. & Henriques, D.Y.P. The effect of visuomotor adaptation on proprioceptive localization: the contributions of perceptual and motor changes. Exp Brain Res 232, 2073–2086 (2014). https://doi.org/10.1007/s00221-014-3896-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-014-3896-y