Roll tilt self-motion direction discrimination training: First evidence for perceptual learning
Tóm tắt
Perceptual learning, the ability to improve the sensitivity of sensory perception through training, has been shown to exist in all sensory systems but the vestibular system. A previous study found no improvement of passive self-motion thresholds in the dark after intense direction discrimination training of either yaw rotations (stimulating semicircular canals) or y-translation (stimulating otoliths). The goal of the present study was to investigate whether perceptual learning of self-motion in the dark would occur when there is a simultaneous otolith and semicircular canal input, as is the case with roll tilt motion stimuli. Blindfolded subjects (n = 10) trained on a direction discrimination task with 0.2-Hz roll tilt motion stimuli (9 h of training, 1,800 trials). Before and after training, motion thresholds were measured in the dark for the trained motion and for three transfer conditions. We found that roll tilt sensitivity in the 0.2-Hz roll tilt condition was increased (i.e., thresholds decreased) after training but not for controls who were not exposed to training. This is the first demonstration of perceptual learning of passive self-motion direction discrimination in the dark. The results have potential therapeutic relevance as 0.2-Hz roll thresholds have been associated with poor performance on a clinical balance test that has been linked to more than a fivefold increase in falls.
Tài liệu tham khảo
Aberg, K. C., Tartaglia, E. M., & Herzog, M. H. (2009). Perceptual learning with Chevrons requires a minimal number of trials, transfers to untrained directions, but does not require sleep. Vision Research, 49(16), 2087-2094.
Agrawal, Y., Bremova, T., Kremmyda, O., Strupp, M., & MacNeilage, P. R. (2013). Clinical testing of otolith function: Perceptual thresholds and myogenic potentials. Journal of the Association for Research in Otolaryngology, 14(6), 905-915.
Agrawal, Y., Carey, J. P., Della Santina, C. C., Schubert, M. C., & Minor, L. B. (2009). Disorders of balance and vestibular function in US adults: Data from the National Health and Nutrition Examination Survey, 2001-2004. Archives of Internal Medicine, 169(10), 938-944.
Agrawal, Y., Zuniga, M. G., Davalos-Bichara, M., Schubert, M. C., Walston, J. D., Hughes, J., & Carey, J. P. (2012). Decline in semicircular canal and otolith function with age. Otology & neurotology: official publication of the American Otological Society, American Neurotology Society [and] European Academy of Otology and Neurotology, 33(5), 832.
Allen, D., Ribeiro, L., Arshad, Q., & Seemungal, B. M. (2017). Age-related vestibular loss: Current understanding and future research directions. Frontiers in Neurology, 7(231).
Atienza, M., Cantero, J. L., & Dominguez-Marin, E. (2002). The time course of neural changes underlying auditory perceptual learning. Learning & Memory, 9(3), 138-150.
Atkinson, J., Braddick, O., & Moar, K. (1977). Development of contrast sensitivity over the first 3 months of life in the human infant. Vision Research, 17(9), 1037-1044.
Barr, D. J., Levy, R., Scheepers, C., & Tily, H. J. (2013). Random effects structure for confirmatory hypothesis testing: Keep it maximal. Journal of Memory and Language, 68(3), 255-278.
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1-48.
Bermúdez Rey, M. C., Clark, T. K., Wang, W., Leeder, T., Bian, Y., & Merfeld, D. M. (2016). Vestibular perceptual thresholds increase above the age of 40. Frontiers in Neurology, 7(162).
Beylergil, S. B., Karmali, F., Wang, W., Bermúdez Rey, M. C., & Merfeld, D. M. (2019). Chapter 18: Vestibular roll tilt thresholds partially mediate age-related effects on balance. Progress in Brain Research, 248, 249-267.
Bremova, T., Caushaj, A., Ertl, M., Strobl, R., Böttcher, N., Strupp, M., & MacNeilage, P. R. (2016). Comparison of linear motion perception thresholds in vestibular migraine and Menière’s disease. European Archives of Oto-Rhino-Laryngology, 273(10), 2931-2939.
Bürkner, P.-C. (2017). brms: An R package for Bayesian multilevel models using Stan. Journal of Statistical Software, 80(1), 1-28.
Chaudhuri, S. E., & Merfeld, D. M. (2013). Signal detection theory and vestibular perception: III. Estimating unbiased fit parameters for psychometric functions. Experimental Brain Research, 225(1), 133-146.
Clark, T. K., Galvan-Garza, R. C., Bermudez Rey, M. C., Yi, Y., & Merfeld, D. M. (2015). Perceptual noise and sensorimotor adaptation. NASA Human Research Program Investigator’s Workshop, Galveston, TX, 13-15 Jan, 2015.
Clark, T. K., & Merfeld, D. M. (2016). Vestibular perceptual noise and adaptation to an altered gravity environment. NASA Human Research Program Investigator’s Workshop, Galveston, TX, 8-11 Feb, 2016.
De Niear, M. A., Noel, J.-P., & Wallace, M. T. (2017). The impact of feedback on the different time courses of multisensory temporal recalibration. Neural Plasticity, 2017.
Dosher, B., & Lu, Z.-L. (2017). Visual perceptual learning and models. Annual Review of Vision Science, 3, 343-363.
Ellis, A. W., Klaus, M. P., & Mast, F. W. (2017). Vestibular cognition: The effect of prior belief on vestibular perceptual decision making. Journal of Neurology, 264(1), 74-80.
Fahle, M. (2005). Perceptual learning: Specificity versus generalization. Current Opinion in Neurobiology, 15(2), 154-160.
Fahle, M., & Edelman, S. (1993). Long-term learning in vernier acuity: Effects of stimulus orientation, range and of feedback. Vision Research, 33(3), 397-412.
Fahle, M., Edelman, S., & Poggio, T. (1995). Fast perceptual learning in hyperacuity. Vision Research, 35(21), 3003-3013.
Fahle, M., & Poggio, T. A. (2002). Perceptual learning. Cambridge, MA: MIT Press.
Gelman, A., & Hill, J. (2007). Data analysis using regression and multilevel/hierarchical models. Cambridge university press.
Gelman, A., Stern, H. S., Carlin, J. B., Dunson, D. B., Vehtari, A., & Rubin, D. B. (2013). Bayesian data analysis. Boca Raton, FL: Chapman and Hall/CRC.
Gibson, E. J. (1969). Principles of perceptual learning and development. Englewood Cliffs, NJ: Prentice Hall.
Gold, J. I., & Watanabe, T. (2010). Perceptual learning. Current Biology, 20(2), R46-R48.
Goldhacker, M., Rosengarth, K., Plank, T., & Greenlee, M. W. (2014). The effect of feedback on performance and brain activation during perceptual learning. Vision Research, 99, 99-110.
Grabherr, L., Nicoucar, K., Mast, F. W., & Merfeld, D. M. (2008). Vestibular thresholds for yaw rotation about an earth-vertical axis as a function of frequency. Experimental Brain Research, 186(4), 677-681.
Guo, J., & Guo, A. (2005). Crossmodal interactions between olfactory and visual learning in Drosophila. Science, 309(5732), 307-310.
Hartmann, M., Furrer, S., Herzog, M. H., Merfeld, D. M., & Mast, F. W. (2013). Self-motion perception training: thresholds Improve in the light but not in the dark. Experimental Brain Research, 226(2), 231-240.
Iwasaki, S., & Yamasoba, T. (2015). Dizziness and imbalance in the elderly: Age-related decline in the vestibular system. Aging and Disease, 6(1), 38.
Jian, B., Shintani, T., Emanuel, B., & Yates, B. (2002). Convergence of limb, visceral, and vertical semicircular canal or otolith inputs onto vestibular nucleus neurons. Experimental Brain Research, 144(2), 247-257.
Karmali, F., Bermúdez Rey, M. C., Clark, T. K., Wang, W., & Merfeld, D. M. (2017). Multivariate analyses of balance test performance, vestibular thresholds, and age. Frontiers in Neurology, 8(578).
Katahira, K. (2016). How hierarchical models improve point estimates of model parameters at the individual level. Journal of Mathematical Psychology, 73, 37-58.
Kingma, H. (2005). Thresholds for perception of direction of linear acceleration as a possible evaluation of the otolith function. BMC Ear, Nose and Throat Disorders, 5(1), 5.
Knoblauch, K., & Maloney, L. T. (2012). Modeling psychophysical data in R (Vol. 32). Springer Science & Business Media.
Kruschke, J. K. (2013). Bayesian estimation supersedes the t test. Journal of Experimental Psychology: General, 142(2), 573.
Lewis, R. F., Priesol, A. J., Nicoucar, K., Lim, K., & Merfeld, D. M. (2011). Dynamic tilt thresholds are reduced in vestibular migraine. Journal of Vestibular Research, 21(6), 323-330.
Lim, K., Karmali, F., Nicoucar, K., & Merfeld, D. M. (2017). Perceptual precision of passive body tilt is consistent with statistically optimal cue integration. Journal of Neurophysiology, 117(5), 2037-2052.
Merfeld, D. M. (2011). Signal detection theory and vestibular thresholds: I. Basic theory and practical considerations. Experimental Brain Research, 210(3-4), 389-405.
Mittelstaedt, H. (1992). Somatic versus vestibular gravity reception in man. Annals of the New York Academy of Sciences, 656(1), 124-139.
Mittelstaedt, H. (1996). Somatic graviception. Biological Psychology, 42(1-2), 53-74.
Moore, D. R., Amitay, S., & Hawkey, D. J. (2003). Auditory perceptual learning. Learning & Memory, 10(2), 83-85.
Moreno, M. M., Linster, C., Escanilla, O., Sacquet, J., Didier, A., & Mandairon, N. (2009). Olfactory perceptual learning requires adult neurogenesis. Proceedings of the National Academy of Sciences, 106(42), 17980-17985.
Nicenboim, B., & Vasishth, S. (2016). Statistical methods for linguistic research: Foundational Ideas—Part II. Language and Linguistics Compass, 10(11), 591-613.
Owen, D. H., & Machamer, P. K. (1979). Bias-free improvement in wine discrimination. Perception, 8(2), 199-209.
Parkosadze, K., Otto, T. U., Malania, M., Kezeli, A., & Herzog, M. H. (2008). Perceptual learning of bisection stimuli under roving: Slow and largely specific. Journal of Vision, 8(1), 5-5.
Pleger, B., Foerster, A.-F., Ragert, P., Dinse, H. R., Schwenkreis, P., Malin, J.-P., Nicolas, V., & Tegenthoff, M. (2003). Functional imaging of perceptual learning in human primary and secondary somatosensory cortex. Neuron, 40(3), 643-653.
Poggio, T., Fahle, M., & Edelman, S. (1992). Fast perceptual learning in visual hyperacuity. Science, 256(5059), 1018-1021.
Roditi, R. E., & Crane, B. T. (2012). Directional asymmetries and age effects in human self-motion perception. Journal of the Association for Research in Otolaryngology, 13(3), 381-401.
Sathian, K., & Zangaladze, A. (1998). Perceptual learning in tactile hyperacuity: Complete intermanual transfer but limited retention. Experimental Brain Research, 118(1), 131-134.
Seitz, A. R., Kim, R., & Shams, L. (2006). Sound facilitates visual learning. Current Biology, 16(14), 1422-1427.
Shams, L., & Seitz, A. R. (2008). Benefits of multisensory learning. Trends in Cognitive Sciences, 12(11), 411-417.
Stan Developent Team. (2018). RStan: The R interface to Stan. R package version 2.17.3.
Valko, Y., Lewis, R. F., Priesol, A. J., & Merfeld, D. M. (2012). Vestibular labyrinth contributions to human whole-body motion discrimination. Journal of Neuroscience, 32(39), 13537-13542.
Vimal, V. P., DiZio, P., & Lackner, J. R. (2017). Learning dynamic balancing in the roll plane with and without gravitational cues. Experimental Brain Research, 235(11), 3495-3503.
Vimal, V. P., Lackner, J. R., & DiZio, P. (2018). Learning dynamic control of body yaw orientation. Experimental Brain Research, 236(5), 1321-1330.
Von Kriegstein, K., & Giraud, A.-L. (2006). Implicit multisensory associations influence voice recognition. PLoS Biology, 4(10), e326.
Wichmann, F. A., & Hill, N. J. (2001). The psychometric function: I. Fitting, sampling, and goodness of fit. Perception & Psychophysics, 63(8), 1293-1313.
Wilson, D. A., & Stevenson, R. J. (2003). The fundamental role of memory in olfactory perception. Trends in Neurosciences, 26(5), 243-247.
Wolfe, J., Kluender, K., Levi, D. M., Bartoshuk, L., Herz, R., Klatzky, R., & Merfeld, D. M. (2018). Chapter 12: Vestibular sensation. Sensation and Perception (pp. 378-419). Cary, NC: Oxford University Press USA.
Yates, B., & Stocker, S. (1998). Integration of somatic and visceral inputs by the brainstem Functional considerations. Experimental Brain Research, 119(3), 269-275.