Abstract
The ability to adapt is critical to survival and varies between individuals. Adaptation of one motor system may be related to the ability to adapt another. This study sought to determine whether phoria adaptation was correlated with the ability to modify the dynamics of disparity vergence. Eye movements from ten subjects were recorded during dynamic disparity vergence modification and phoria adaptation experiments. Two different convergent stimuli were presented during the dynamic vergence modification experiment: a test stimulus (4° step) and a conditioning stimulus (4° double step). Dynamic disparity vergence responses were quantified by measuring the peak velocity (°/s). Phoria adaptation experiments measured the changes in phoria over a 5-min period of sustained fixation. The maximum velocity of phoria adaptation was determined from an exponential fit of the phoria data points. Phoria and dynamic disparity vergence peak velocity were both significantly modified (P < 0.001). The maximum velocity of phoria adaptation was significantly correlated with the changes in convergence peak velocity (r > 0.89; P < 0.001). There was a strong correlation between the ability to adaptively adjust two different oculomotor parameters: a tonic and dynamic component. Future studies should investigate additional interactions between these parameters, and the ability to adaptively change other oculomotor systems such as the saccadic or smooth pursuit system. Understanding the ability to modify phoria, dynamic disparity vergence, and other oculomotor parameters can yield insights into the plasticity of short-term adaptation mechanisms.
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References
Albano JE (1996) Adaptive changes in saccade amplitude: oculocentric or orbitocentric mapping? Vision Res 36:2087–2098. doi:0042-6989(96)89627-1
Alvarez TL, Semmlow JL, Yuan W, Munoz P (2002) Comparison of disparity vergence system responses to predictable and non-predictable stimulations. Curr Pscyhol Cogn 21:243–261
Alvarez TL, Bhavsar M, Semmlow JL, Bergen MT, Pedrono C (2005) Short-term predictive changes in the dynamics of disparity vergence eye movements. J Vis 5:640–649. doi:10:1167/5.7.4/5/7/4/
Alvarez TL, Han SJ, Kania C et al. (2009) Adaptation to progressive lenses by presbyopes. In: NER ‘09. 4th international IEEE/EMBS conference Antalya, Turkey
Alvarez TL, Vicci VR, Alkan Y et al (2010) Vision therapy in adults with convergence insufficiency: clinical and functional magnetic resonance imaging measures. Optom Vis Sci 87:E985–E1002. doi:10.1097/OPX.0b013e3181fef1aa
Bahill AT, Kallman JS, Lieberman JE (1982) Frequency limitations of the two-point central difference differentiation algorithm. Biol Cybern 45:1–4
Brautaset RL, Jennings JA (2005) Distance vergence adaptation is abnormal in subjects with convergence insufficiency. Ophthalmic Physiol Opt 25:211–214. doi:10.1111/j.1475-1313.2005.00274.x
Brautaset RL, Jennings AJ (2006) Effects of orthoptic treatment on the CA/C and AC/A ratios in convergence insufficiency. Invest Ophthalmol Vis Sci 47:2876–2880. doi:10.1167/iovs.04-1372
Cheng D, Schmid KL, Woo GC (2008) The effect of positive-lens addition and base-in prism on accommodation accuracy and near horizontal phoria in Chinese myopic children. Ophthalmic Physiol Opt 28:225–237. doi:10.1111/j.1475-1313.2008.00560.x
Churchland AK, Lisberger SG (2002) Gain control in human smooth-pursuit eye movements. J Neurophysiol 87:2936–2945
Dash S, Catz N, Dicke PW, Thier P (2010) Specific vermal complex spike responses build up during the course of smooth-pursuit adaptation, paralleling the decrease of performance error. Exp Brain Res 205:41–55. doi:10.1007/s00221-010-2331-2
Ditterich J, Eggert T, Straube A (2000) The role of the attention focus in the visual information processing underlying saccadic adaptation. Vision Res 40:1125–1134. doi:S0042-6989(00)00018-3
Fogt N, Toole AJ (2001) The effect of saccades and brief fusional stimuli on phoria adaptation. Optom Vis Sci 78:815–824. doi:00006324-200111000-00011
Frens MA, van Opstal AJ (1994) Transfer of short-term adaptation in human saccadic eye movements. Exp Brain Res 100:293–306
Fukushima K, Tanaka M, Suzuki Y, Fukushima J, Yoshida T (1996) Adaptive changes in human smooth pursuit eye movement. Neurosci Res 25:391–398. doi:S0168010296010681
Gilbert PF, Thach WT (1977) Purkinje cell activity during motor learning. Brain Res 128:309–328. doi:0006-8993(77)90997-0
Han SJ, Guo Y, Granger-Donetti B, Vicci VR, Alvarez TL (2010) Quantification of heterophoria and phoria adaptation using an automated objective system compared to clinical methods. Ophthalmic Physiol Opt 30:95–107. doi:10.1111/j.1475-1313.2009.00681.x
Havermann K, Lappe M (2010) The influence of the consistency of postsaccadic visual errors on saccadic adaptation. J Neurophysiol 103:3302–3310. doi:10.1152/jn.00970.2009
Horng JL, Semmlow JL, Hung GK, Ciuffreda KJ (1998) Initial component control in disparity vergence: a model-based study. IEEE Trans Biomed Eng 45:249–257. doi:10.1109/10.661273
Hung GK, Semmlow JL, Ciuffreda KJ (1983) Identification of accommodative vergence contribution to the near response using response variance. Invest Ophthalmol Vis Sci 24:772–777
Iwamoto Y, Kaku Y (2010) Saccade adaptation as a model of learning in voluntary movements. Exp Brain Res 204:145–162. doi:10.1007/s00221-010-2314-3
Jainta S, Hoormann J, Jaschinski W (2007) Objective and subjective measures of vergence step responses. Vision Res 47:3238–3246. doi:10.1016/j.visres.2007.05.006
Jiang BC, Tea YC, O’Donnell D (2007) Changes in accommodative and vergence responses when viewing through near addition lenses. Optometry 78:129–134. doi:10.1016/j.optm.2006.08.017
Joiner WM, Fitzgibbon EJ, Wurtz RH (2010) Amplitudes and directions of individual saccades can be adjusted by corollary discharge. J Vis 10(2):22.1–2212. doi:10.1167/10.2.22/10/2/22/
Jones R (1977) Anomalies of disparity detection in the human visual system. J Physiol 264:621–640
Kim EH, Granger-Donetti B, Vicci VR, Alvarez TL (2010) The relationship between phoria and the ratio of convergence peak velocity to divergence peak velocity. Invest Ophthalmol Vis Sci. doi:10.1167/iovs.09-4560
Kojima Y, Soetedjo T, Fuch AF (2010) Changes in simple spike activity of some Purkinje cells in the oculomotor vermis during saccade adaptation are appropriate to participate in motor learning. J Neurosci 30(10):3715–3727
Lee YY, Granger-Donetti B, Chang C, Alvarez TL (2009) Sustained convergence induced changes in phoria and divergence dynamics. Vis Res 49:2960–2972. doi:10.1016/j.visres.2009.09.013
Leigh RJ, Zee DS (2006) The neurology of eye movements. Oxford University Press, Oxford
Marr D (1969) A theory of cerebellar cortex. J Physiol 202:437–470
Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT (1996) Throwing while looking through prisms. I. Focal olivocerebellar lesions impair adaptation. Brain 119(Pt 4):1183–1198
Medina JF, Lisberger SG (2008) Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys. Nat Neurosci 11:1185–1192. doi:10.1038/nn.2197
Munoz P, Semmlow JL, Yuan W, Alvarez TL (1999) Short term modification of disparity vergence eye movements. Vis Res 39:1695–1705. doi:S0042-6989(98)00206-5
Nitta T, Akao T, Kurkin S, Fukushima K (2008a) Involvement of the cerebellar dorsal vermis in vergence eye movements in monkeys. Cereb Cortex 18:1042–1057. doi:10.1093/cercor/bhm143
Nitta T, Akao T, Kurkin S, Fukushima K (2008b) Vergence eye movement signals in the cerebellar dorsal vermis. Prog Brain Res 171:173–176. doi:10.1016/S0079-6123(08)00623-7
North RV, Henson DB (1982) Effect of orthoptics upon the ability of patients to adapt to prism-induced heterophoria. Am J Optom Physiol Opt 59:983–986
Ojakangas CL, Ebner TJ (1992) Purkinje cell complex and simple spike changes during a voluntary arm movement learning task in the monkey. J Neurophysiol 68:2222–2236
Ono S, Mustari MJ (2010) Visual error signals from the pretectal nucleus of the optic tract guide motor learning for smooth pursuit. J Neurophysiol 103:2889–2899. doi:10.1152/jn.01024.2009
Optican LM, Robinson DA (1980) Cerebellar-dependent adaptive control of primate saccadic system. J Neurophysiol 44:1058–1076
Otto JM, Bach M, Kommerell G (2009) Vergence position of rest: spontaneous variability. Strabismus 17:143–147. doi:10.3109/09273970903295405
Pelisson D, Alahyane N, Panouilleres M, Tilikete C (2010) Sensorimotor adaptation of saccadic eye movements. Neurosci Biobehav Rev 34:1103–1120. doi:10.1016/j.neubiorev.2009.12.010
Rolfs M, Knapen T, Cavanagh P (2010) Global saccadic adaptation. Vision Res 50:1882–1890. doi:10.1016/j.visres.2010.06.010
Rosenfield M, Rappon JM, Carrel MF (2000) Vergence adaptation and the clinical AC/A ratio. Ophthalmic Physiol Opt 20:207–211. doi:S0275-5408(99)00051-4
Schor CM (2009) Neuromuscular plasticity and rehabilitation of the ocular near response. Optom Vis Sci 86:E788–E802. doi:10.1097/OPX.0b013e3181ae00a5
Schubert MC, Zee DS (2010) Saccade and vestibular ocular motor adaptation. Restor Neurol Neurosci 28:9–18. doi:10.3233/RNN-2010-0523
Scudder CA, Batourina EY, Tunder GS (1998) Comparison of two methods of producing adaptation of saccade size and implications for the site of plasticity. J Neurophysiol 79:704–715
Semmlow JL, Gauthier GM, Vercher JL (1989) Mechanisms of short-term saccadic adaptation. J Exp Psychol Hum Percept Perform 15:249–258
Semmlow JL, Yuan W, Alvarez TL (2002) Short-term adaptive control processes in vergence eye movements. Curr Psych Cog 21(4–5):243–261
Straube A, Fuchs AF, Usher S, Robinson FR (1997) Characteristics of saccadic gain adaptation in rhesus macaques. J Neurophysiol 77:874–895
Tabata H, Miura K, Kawano K (2008) Trial-by-trial updating of the gain in preparation for smooth pursuit eye movement based on past experience in humans. J Neurophysiol 99: 747–758. doi:10.1152/jn.00714.2007
Takagi M, Oyamada H, Abe H et al (2001) Adaptive changes in dynamic properties of human disparity-induced vergence. Invest Ophthalmol Vis Sci 42:1479–1486
Takagi M, Tamargo R, Zee DS (2003) Effects of lesions of the cerebellar oculomotor vermis on eye movements in primate: binocular control. Prog Brain Res 142:19–33. doi:10.1016/S0079-6123(03)42004-9
Thiagarajan P, Lakshminarayanan V, Bobier WR (2010) Effect of vergence adaptation and positive fusional vergence training on oculomotor parameters. Optom Vis Sci 87:487–493. doi:10.1097/OPX.0b013e3181e19ec2
Tian J, Ethier V, Shadmehr R, Fujita M, Zee DS (2009) Some perspectives on saccade adaptation. Ann NY Acad Sci 1164:166–172. doi:10.1111/j.1749-6632.2009.03853.x
van Leeuwen AF, Westen MJ, van der Steen J, de Faber JT, Collewijn H (1999) Gaze-shift dynamics in subjects with and without symptoms of convergence insufficiency: influence of monocular preference and the effect of training. Vis Res 39:3095–3107. doi:S0042-6989(99)00066-8
Wolf KS, Bedell HE, Pedersen SB (1990) Relations between accommodation and vergence in darkness. Optom Vis Sci 67:89–93
Yang J, Lisberger SG (2009) Relationship between adapted neural population responses in MT and motion adaptation in speed and direction of smooth-pursuit eye movements. J Neurophysiol 101:2693–2707. doi:10.1152/jn.00061.2009
Yuan W, Semmlow JL (2000) The influence of repetitive eye movements on vergence performance. Vis Res 40:3089–3098. doi:S0042-6989(00)00162-0
Yuan W, Semmlow JL, Muller-Munoz P (2001) Model-based analysis of dynamics in vergence adaptation. IEEE Trans Biomed Eng 48:1402–1411. doi:10.1109/10.966599
Zee DS, Fitzgibbon EJ, Optican LM (1992) Saccade-vergence interactions in humans. J Neurophysiol 68:1624–1641
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This research was supported in part by NSF CAREER BES-044713 and Essilor International.
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Kim, E.H., Vicci, V.R., Granger-Donetti, B. et al. Short-term adaptations of the dynamic disparity vergence and phoria systems. Exp Brain Res 212, 267–278 (2011). https://doi.org/10.1007/s00221-011-2727-7
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DOI: https://doi.org/10.1007/s00221-011-2727-7