Abstract
Standard visually guided reaching begins with foveation of a target of interest followed by an arm movement to the same spatial location. However, many visually guided arm movements, as well as a majority of imaging studies examining such movements, require participants to perform non-standard visuomotor mappings where the locations of gaze and arm movements are spatially dissociated (e.g. gaze fixation peripheral to the target of a reaching movement, or use of a tool such as a joystick while viewing stimuli on a screen). In this study, we compare brain activity associated with the production of standard visually guided arm movements to activity during a visuomotor mapping where saccades and reaches were made in different spatial planes. Multi-voxel pattern analysis revealed that while spatial patterns of voxel activity remain quite similar for the two visuomotor mappings during presentation of a cue for movement, patterns of activity become increasingly more discriminative throughout the brain as planning progresses toward motor execution. Decoding of the visuomotor mappings occurs throughout visuomotor-related regions of the brain including the premotor, primary motor and somatosensory, posterior parietal, middle occipital, and medial occipital cortices, and in the cerebellum. These results show that relative to standard visuomotor tasks, activity differs substantially in areas throughout the brain when a task requires an implicit sensorimotor recalibration.
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References
Batista AP, Buneo CA, Snyder LH, Andersen RA (1999) Reach plans in eye-centered coordinates. Science 285:257–260. https://doi.org/10.1126/science.285.5425.257
Bock O, Girgenrath M (2006) Relationship between sensorimotor adaptation and cognitive functions in younger and older subjects. Exp Brain Res Hirnforschung Exp Cerebrale 169:400–406. https://doi.org/10.1007/s00221-005-0153-4
Brown J, Dalecki M, Hughes C et al (2015) Cognitive-motor integration deficits in young adult athletes following concussion. BMC Sports Sci Med Rehabilit 7:1. https://doi.org/10.1186/s13102-015-0019-4
Buneo CA, Batista AP, Jarvis MR, Andersen RA (2008) Time-invariant reference frames for parietal reach activity. Exp Brain Res 188:77–89. https://doi.org/10.1007/s00221-008-1340-x
Buxbaum LJ, Coslett HB (1997) Subtypes of optic ataxia: reframing the disconnection account. Neurocase 3:159–166. https://doi.org/10.1093/neucas/3.3.159
Carey DP, Coleman RJ, Della Sala S (1997) Magnetic misreaching. Cortex 33:639–652
Chen Y, Monaco S, Byrne P et al (2014) Allocentric versus egocentric representation of remembered reach targets in human cortex. J Neurosci 34:12515–12526. https://doi.org/10.1523/JNEUROSCI.1445-14.2014
Cisek P, Kalaska JF (2005) Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action. Neuron 45:801–814. https://doi.org/10.1016/j.neuron.2005.01.027
Coallier É, Michelet T, Kalaska JF (2015) Dorsal premotor cortex: neural correlates of reach target decisions based on a color-location matching rule and conflicting sensory evidence. J Neurophysiol 113:3543–3573. https://doi.org/10.1152/jn.00166.2014
Cohen YE, Andersen RA (2002) A common reference frame for movement plans in the posterior parietal cortex. Nat Rev 3:553–562. https://doi.org/10.1038/nrn873
Coutanche MN (2013) Distinguishing multi-voxel patterns and mean activation: why, how, and what does it tell us? Cogn Affect Behav Neurosci 13:667–673. https://doi.org/10.3758/s13415-013-0186-2
Crawford JD, Medendorp WP, Marotta JJ (2004) Spatial transformations for eye–hand coordination. J Neurophysiol 92:10–19. https://doi.org/10.1152/jn.00117.2004
Dalecki M, Albines D, Macpherson A, Sergio LE (2016) Prolonged cognitive–motor impairments in children and adolescents with a history of concussion. Concussion. https://doi.org/10.2217/cnc-2016-0001
De Martino F, Valente G, Staeren N et al (2008) Combining multivariate voxel selection and support vector machines for mapping and classification of fMRI spatial patterns. Neuroimage 43:44–58. https://doi.org/10.1016/j.neuroimage.2008.06.037
Filimon F, Nelson JD, Huang RS, Sereno MI (2009) Multiple parietal reach regions in humans: cortical representations for visual and proprioceptive feedback during on-line reaching. J Neurosci 29:2961–2971. https://doi.org/10.1523/JNEUROSCI.3211-08.2009
Fisk JD, Goodale MA (1985) The organization of eye and limb movements during unrestricted reaching to targets in contralateral and ipsilateral visual space. Exp Brain Res 60:159–178. https://doi.org/10.1007/BF00237028
Frassinetti F, Bonifazi S, Làdavas E (2007) The influence of spatial coordinates in a case of an optic ataxia-like syndrome following cerebellar and thalamic lesion. Cogn Neuropsychol 24:324–337. https://doi.org/10.1080/02643290701275857
Genovesio A, Brasted PJ, Mitz AR, Wise SP (2005) Prefrontal cortex activity related to abstract response strategies. Neuron 47:307–320. https://doi.org/10.1016/j.neuron.2005.06.006
Gorbet DJ, Sergio LE (2007) Preliminary sex differences in human cortical BOLD fMRI activity during the preparation of increasingly complex visually guided movements. Eur J Neurosci 25:1228–1239. https://doi.org/10.1111/j.1460-9568.2007.05358.x
Gorbet DJ, Sergio LE (2016) Don’t watch where you’re going: the neural correlates of decoupling eye and arm movements. Behav Brain Res. https://doi.org/10.1016/j.bbr.2015.11.012
Gorbet DJ, Staines WR (2011) Inhibition of contralateral premotor cortex delays visually guided reaching movements in men but not in women. Exp Brain Res 212:315–325. https://doi.org/10.1007/s00221-011-2731-y
Gorbet DJ, Staines WR, Sergio LE (2004) Brain mechanisms for preparing increasingly complex sensory to motor transformations. Neuroimage 23:1100–1111. https://doi.org/10.1016/j.neuroimage.2004.07.043
Gorbet DJ, Mader LB, Richard Staines W (2010) Sex-related differences in the hemispheric laterality of slow cortical potentials during the preparation of visually guided movements. Exp Brain Res 202:633–646. https://doi.org/10.1007/s00221-010-2170-1
Granek JA, Sergio LE (2015) Evidence for distinct brain networks in the control of rule-based motor behavior. J Neurophysiol 114:1298–1309. https://doi.org/10.1152/jn.00233.2014
Granek JA, Gorbet DJ, Sergio LE (2010) Extensive video-game experience alters cortical networks for complex visuomotor transformations. Cortex 46:1165–1177. https://doi.org/10.1016/j.cortex.2009.10.009
Granek J, Pisella L, Stemberger J et al (2013) Decoupled visually-guided reaching in optic ataxia: differences in motor control between canonical and non-canonical orientations in space. PLoS One 8:1–18. https://doi.org/10.1371/journal.pone.0086138
Grigorova V, Bock O, Ilieva M, Schmitz G (2013) Directional adaptation of reactive saccades and hand pointing movements is not independent. J Mot Behav 45:101–106. https://doi.org/10.1080/00222895.2012.750590
Guyon I, Elisseeff A (2003) An introduction to variable and feature selection. J Mach Learn Res 3:1157–1182
Hawkins KM, Sergio LE (2014) Visuomotor impairments in older adults at increased Alzheimer’s disease risk. J Alzheimers Dis 42:607–621. https://doi.org/10.3233/JAD-140051
Hawkins KM, Sayegh P, Yan X et al (2013) Neural activity in superior parietal cortex during rule-based visual-motor transformations. J Cogn Neurosci 25:436–454. https://doi.org/10.1162/jocn_a_00318
Hawkins KM, Goyal AI, Sergio LE (2015) Diffusion tensor imaging correlates of cognitive-motor decline in normal aging and increased Alzheimer’s disease risk. J Alzheimer’s Dis. https://doi.org/10.3233/JAD-142079
Henriques DY, Cressman EK (2012) Visuomotor adaptation and proprioceptive recalibration. J Mot Behav 44:435–444. https://doi.org/10.1080/00222895.2012.659232
Heuer H, Hegele M (2011) Generalization of implicit and explicit adjustments to visuomotor rotations across the workspace in younger and older adults. J Neurophysiol 106:2078–2085. https://doi.org/10.1152/jn.00043.2011
Hurtubise J, Gorbet D, Hamandi Y et al (2016) The effect of concussion history on cognitive-motor integration in elite hockey players. Concussion 1:CNC17. https://doi.org/10.2217/cnc-2016-0006
Kalaska JF, Hyde ML (1985) Area 4 and area 5: differences between the load direction-dependent discharge variability of cells during active postural fixation. Exp Brain Res 59:197–202
Klaes C, Westendorff S, Chakrabarti S, Gail A (2011) Choosing goals, not rules: deciding among rule-based action plans. Neuron 70:536–548. https://doi.org/10.1016/j.neuron.2011.02.053
Kröller J, De Graaf JB, Prablanc C, Pélisson D (1999) Effects of short term adaptation of saccadic gaze amplitude on hand-pointing movements. Exp Brain Res 124:351–362. https://doi.org/10.1007/s002210050632
Lee D, Poizner H, Corcos DM, Henriques DY (2014) Unconstrained reaching modulates eye–hand coupling. Exp Brain Res 232:211–223. https://doi.org/10.1007/s00221-013-3732-9
McDougle SD, Bond KM, Taylor JA (2015) Explicit and implicit processes constitute the fast and slow processes of sensorimotor learning. J Neurosci 35:9568–9579. https://doi.org/10.1523/JNEUROSCI.5061-14.2015
McNay EC, Willingham DB (1998) Deficit in learning of a motor skill requiring strategy, but not of perceptuomotor recalibration, with aging. Learn Mem 4:411–420
Medendorp WP, Goltz HC, Vilis T (2006) Directional selectivity of BOLD activity in human posterior parietal cortex for memory-guided double-step saccades. J Neurophysiol 95:1645–1655. https://doi.org/10.1152/jn.00905.2005
Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202. https://doi.org/10.1146/annurev.neuro.24.1.167
Misaki M, Kim Y, Bandettini PA, Kriegeskorte N (2010) Comparison of multivariate classifiers and response normalizations for pattern-information fMRI. Neuroimage 53:103–118. https://doi.org/10.1016/j.neuroimage.2010.05.051
Mushiake H, Fujii N, Tanji J (1996) Visually guided saccade versus eye-hand reach: contrasting neuronal activity in the cortical supplementary and frontal eye fields. J Neurophysiol 75:2187–2191
Neggers SF, Bekkering H (2000) Gaze anchoring to a pointing target is present during the entire pointing movement and is driven by a non-visual signal. J Neurophysiol 83:961–970
Pellijeff A, Bonilha L, Morgan PS et al (2006) Parietal updating of limb posture: an event-related fMRI study. Neuropsychologia 44:2685
Prablanc C, Echallier JF, Komilis E, Jeannerod M (1979) Optimal response of eye and hand motor systems in pointing at a visual target. I. Spatio-temporal characteristics of eye and hand movements and their relationships when varying the amount of visual information. Biol Cybern 35:113–124
Redding GM, Wallace B (1993) Adaptive coordination and alignment of eye and hand. J Mot Behav 25:75–88. https://doi.org/10.1080/00222895.1993.9941642
Reyes-Puerta V, Philipp R, Lindner W, Hoffmann K-P (2010) Role of the rostral superior colliculus in gaze anchoring during reach movements. J Neurophysiol 103:3153–3166. https://doi.org/10.1152/jn.00989.2009
Rowe J, Hughes L, Eckstein D, Owen AM (2008) Rule-selection and action-selection have a shared neuroanatomical basis in the human prefrontal and parietal cortex. Cereb Cortex 18:2275–2285. https://doi.org/10.1093/cercor/bhm249
Salek Y, Anderson ND, Sergio L (2011) Mild cognitive impairment is associated with impaired visual-motor planning when visual stimuli and actions are incongruent. Eur Neurol 66:283–293
Sayegh PF, Hawkins KM, Hoffman KL, Sergio LE (2013) Differences in spectral profiles between rostral and caudal premotor cortex when hand-eye actions are decoupled. J Neurophysiol 110:952–963. https://doi.org/10.1152/jn.00764.2012
Sayegh PF, Hawkins KM, Neagu B et al (2014) Decoupling the actions of the eyes from the hand alters beta and gamma synchrony within SPL. J Neurophysiol. https://doi.org/10.1152/jn.00793.2013
Sayegh PF, Gorbet DJ, Hawkins KM et al (2017) The contribution of different cortical regions to the control of spatially decoupled eye–hand coordination. J Cogn Neurosci 29:1194–1211. https://doi.org/10.1162/jocn_a_01111
Scott SH, Sergio LE, Kalaska JF (1997) Reaching movements with similar hand paths but different arm orientations. II. Activity of individual cells in dorsal premotor cortex and parietal area 5. J Neurophysiol 78:2413–2426
Smith S, Nichols T (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluter inference. Neuroimage 44:83–98
Smith MA, Ghazizadeh A, Shadmehr R (2006) Interacting adaptive processes with different timescales underlie short-term motor learning. PLoS Biol 4:1035–1043. https://doi.org/10.1063/1.2184639
Snyder LH, Batista AP, Andersen RA (2000) Saccade-related activity in the parietal reach region. J Neurophysiol 83:1099–1102. https://doi.org/10.1152/jn.2000.83.2.1099
Song J-H, McPeek RM (2010) Roles of narrow- and broad-spiking dorsal premotor area neurons in reach target selection and movement production. J Neurophysiol 103:2124–2138. https://doi.org/10.1152/jn.00238.2009
Staeren N, Renvall H, De Martino F et al (2009) Sound categories are represented as distributed patterns in the human auditory cortex. Curr Biol 19:498–502. https://doi.org/10.1016/j.cub.2009.01.066
Taylor JA, Krakauer JW, Ivry RB (2014) Explicit and implicit contributions to learning in a sensorimotor adaptation task. J Neurosci 34:3023–3032. https://doi.org/10.1523/JNEUROSCI.3619-13.2014
Tippett WJ, Sergio LE (2006) Visuomotor integration is impaired in early stage Alzheimer’s disease. Brain Res 1102:92–102. https://doi.org/10.1016/j.brainres.2006.04.049
Tippett WJ, Sergio LE, Black SE (2012) Compromised visually guided motor control in individuals with Alzheimer’s disease: can reliable distinctions be observed? J Clin Neurosci 19:655–660. https://doi.org/10.1016/j.jocn.2011.09.013
Wallis JD, Miller EK (2003) From rule to response: neuronal processes in the premotor and prefrontal cortex. J Neurophysiol 90:1790–1806. https://doi.org/10.1152/jn.00086.2003
Wise SP, di Pellegrino G, Boussaoud D (1996) The premotor cortex and nonstandard sensorimotor mapping. Can J Physiol Pharmacol 74:469–482
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The funding was received by Natural Sciences and Engineering Research Council of Canada (NSERC) (Grant no. 227220-2011).
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Gorbet, D.J., Sergio, L.E. Looking up while reaching out: the neural correlates of making eye and arm movements in different spatial planes. Exp Brain Res 237, 57–70 (2019). https://doi.org/10.1007/s00221-018-5395-z
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DOI: https://doi.org/10.1007/s00221-018-5395-z