Perceptual decisions about object shape bias visuomotor coordination during rapid interception movements.

Visual processing in parietal areas of the dorsal stream facilitates sensorimotor transformations for rapid movement. This action-related visual processing is hypothesized to play a distinct functional role from the perception-related processing in the ventral stream. However, it is unclear how the two streams interact when perceptual identification is a prerequisite to executing an accurate movement. In the current study, we investigated how perceptual decision-making involving the ventral stream influences arm and eye movement strategies. Participants (N = 26) moved a robotic manipulandum using right whole-arm movements to rapidly reach a stationary object or intercept a moving object on an augmented-reality display. On some blocks of trials, participants needed to identify the shape of the object (circle or ellipse) as a cue to either hit the object (circle) or move to a pre-defined location away from the object (ellipse). We found that during perceptual decision-making, there was an increased urgency to act during interception movements relative to reaching, which was associated with more decision errors. Faster hand reaction times were associated with a strategy to adjust the movement post-initiation, and this strategy was more prominent during interception. Saccadic reaction times were faster and initial saccadic peak velocity, initial gaze lags, and gains greater during decisions, suggesting that eye movements adapt to perceptual decision-making requirements. Together, our findings suggest that the integration of ventral stream information with visuomotor planning depends on imposed (or perceived) task demands.

[1]  Leslie G. Ungerleider,et al.  Object vision and spatial vision: two cortical pathways , 1983, Trends in Neurosciences.

[2]  U. Castiello,et al.  Cross-talk connections underlying dorsal and ventral stream integration during hand actions , 2018, Cortex.

[3]  N. Kanwisher,et al.  The lateral occipital complex and its role in object recognition , 2001, Vision Research.

[4]  Eli Brenner,et al.  The latency for correcting a movement depends on the visual attribute that defines the target , 2008, Experimental Brain Research.

[5]  Mikhail Katkov,et al.  Singularities in the inverse modeling of contrast discrimination and ways to avoid them , 2010 .

[6]  John H. R. Maunsell,et al.  Shape selectivity in primate lateral intraparietal cortex , 1998, Nature.

[7]  J. Sharpe,et al.  Vertical vestibulo-ocular reflex, smooth pursuit and eye-head tracking dysfunction in internuclear ophthalmoplegia. , 1988, Brain : a journal of neurology.

[8]  S. Kastner,et al.  Two hierarchically organized neural systems for object information in human visual cortex , 2008, Nature Neuroscience.

[9]  K. Nakayama,et al.  Hidden cognitive states revealed in choice reaching tasks , 2009, Trends in Cognitive Sciences.

[10]  Craig S. Chapman,et al.  Decision-making in sensorimotor control , 2018, Nature Reviews Neuroscience.

[11]  J. Culham,et al.  The role of parietal cortex in visuomotor control: What have we learned from neuroimaging? , 2006, Neuropsychologia.

[12]  T. Schmidt The Finger in Flight: Real-Time Motor Control by Visually Masked Color Stimuli , 2002, Psychological science.

[13]  Tarkeshwar Singh,et al.  A geometric method for computing ocular kinematics and classifying gaze events using monocular remote eye tracking in a robotic environment , 2016, Journal of NeuroEngineering and Rehabilitation.

[14]  J. Vercher,et al.  The role of ocular muscle proprioception in visual localization of targets. , 1990, Science.

[15]  J. Bullier,et al.  Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  Christopher M. Perry,et al.  A novel computational model to probe visual search deficits during motor performance. , 2017, Journal of neurophysiology.

[17]  Stephen G Lisberger,et al.  Visual Guidance of Smooth Pursuit Eye Movements. , 2015, Annual review of vision science.

[18]  M. Davare,et al.  Temporal Dissociation between Hand Shaping and Grip Force Scaling in the Anterior Intraparietal Area , 2007, The Journal of Neuroscience.

[19]  F. Lacquaniti,et al.  The role of preparation in tuning anticipatory and reflex responses during catching , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  Kathleen E Cullen,et al.  Gaze-, eye-, and head-movement dynamics during closed- and open-loop gaze pursuit. , 2002, Journal of neurophysiology.

[21]  Eli Brenner,et al.  Sources of variability in interceptive movements , 2009, Experimental Brain Research.

[22]  G. Rizzolatti,et al.  Two different streams form the dorsal visual system: anatomy and functions , 2003, Experimental Brain Research.

[23]  D. Wolpert,et al.  Changing your mind: a computational mechanism of vacillation , 2009, Nature.

[24]  Steven A. Jax,et al.  The problem of serial order in behavior: Lashley's legacy. , 2007, Human movement science.

[25]  Miriam Reiner,et al.  Multisensory enhancement: gains in choice and in simple response times , 2008, Experimental Brain Research.

[26]  G. Barnes,et al.  Independent control of head and gaze movements during head‐free pursuit in humans , 1999, The Journal of physiology.

[27]  E. Brenner,et al.  A visual illusion that influences perception and action through the dorsal pathway , 2019, Communications Biology.

[28]  S G Lisberger,et al.  Visual motion processing for the initiation of smooth-pursuit eye movements in humans. , 1986, Journal of neurophysiology.

[29]  M. Tanaka,et al.  Latency of saccades during smooth-pursuit eye movement in man Directional asymmetries , 1998, Experimental Brain Research.

[30]  David Thura Decision urgency invigorates movement in humans , 2020, Behavioural Brain Research.

[31]  Stefan Glasauer,et al.  Gain Control in Predictive Smooth Pursuit Eye Movements: Evidence for an Acceleration-Based Predictive Mechanism , 2017, eNeuro.

[32]  Massimiliano Pastore,et al.  Overlapping: a R package for Estimating Overlapping in Empirical Distributions , 2018, J. Open Source Softw..

[33]  Karolina M. Lempert,et al.  Modulation of Saccade Vigor during Value-Based Decision Making , 2015, The Journal of Neuroscience.

[34]  B. Day,et al.  Voluntary modification of automatic arm movements evoked by motion of a visual target , 1999, Experimental Brain Research.

[35]  G. Barnes,et al.  Cognitive processes involved in smooth pursuit eye movements , 2008, Brain and Cognition.

[36]  Manuel Spitschan,et al.  Photoreceptor inputs to pupil control , 2019, Journal of vision.

[37]  S. Thorpe,et al.  Seeking Categories in the Brain , 2001, Science.

[38]  Leslie G. Ungerleider,et al.  The neural systems that mediate human perceptual decision making , 2008, Nature Reviews Neuroscience.

[39]  Stephen G Lisberger,et al.  Gain control in human smooth-pursuit eye movements. , 2002, Journal of neurophysiology.

[40]  Sae Franklin,et al.  Temporal Evolution of Spatial Computations for Visuomotor Control , 2016, The Journal of Neuroscience.

[41]  J F Kalaska,et al.  Integration of predictive feedforward and sensory feedback signals for online control of visually guided movement. , 2009, Journal of neurophysiology.

[42]  Keiji Tanaka,et al.  Neural representation for object recognition in inferotemporal cortex , 2016, Current Opinion in Neurobiology.

[43]  Adrian M. Haith,et al.  Motor planning flexibly optimizes performance under uncertainty about task goals , 2017, Nature Communications.

[44]  S. McKee,et al.  Visual acuity in the presence of retinal-image motion. , 1975, Journal of the Optical Society of America.

[45]  G. Barnes,et al.  Visual-vestibular interaction in the control of head and eye movement: The role of visual feedback and predictive mechanisms , 1993, Progress in neurobiology.

[46]  M. Davare,et al.  Interactions between dorsal and ventral streams for controlling skilled grasp , 2015, Neuropsychologia.

[47]  Paul Krappmann,et al.  PII: S0042-6989(98)00101-1 , 1998 .

[48]  Daniel M Wolpert,et al.  Grip force when reaching with target uncertainty provides evidence for motor optimization over averaging , 2017, Scientific Reports.

[49]  E. Ludvigh,et al.  Study of visual acuity during the ocular pursuit of moving test objects. I. Introduction. , 1958, Journal of the Optical Society of America.

[50]  Karl R. Gegenfurtner,et al.  Object recognition during foveating eye movements , 2009, Vision Research.

[51]  C. Bruce,et al.  Deficits in smooth-pursuit eye movements after muscimol inactivation within the primate's frontal eye field. , 1998, Journal of neurophysiology.

[52]  Benoit Cottereau,et al.  The time course of shape discrimination in the human brain , 2013, NeuroImage.

[53]  G. Rizzolatti,et al.  Motor and cognitive functions of the ventral premotor cortex , 2002, Current Opinion in Neurobiology.

[54]  L. Selen,et al.  Deliberation in the Motor System: Reflex Gains Track Evolving Evidence Leading to a Decision , 2012, The Journal of Neuroscience.

[55]  Miriam Spering,et al.  Decoding go/no-go decisions from eye movements. , 2019, Journal of vision.

[56]  J. Kalaska,et al.  Neural mechanisms for interacting with a world full of action choices. , 2010, Annual review of neuroscience.

[57]  R. Desimone,et al.  Shape recognition and inferior temporal neurons. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[58]  John W. Krakauer,et al.  Hedging Your Bets: Intermediate Movements as Optimal Behavior in the Context of an Incomplete Decision , 2015, PLoS Comput. Biol..

[59]  E. G. Keating,et al.  Frontal eye field lesions impair predictive and visually-guided pursuit eye movements , 2004, Experimental Brain Research.

[60]  Jonathan Winawer,et al.  A Major Human White Matter Pathway Between Dorsal and Ventral Visual Cortex. , 2016, Cerebral cortex.

[61]  K. Nakayama,et al.  Target selection in visual search as revealed by movement trajectories , 2008, Vision Research.

[62]  A. Haith,et al.  Independence of Movement Preparation and Movement Initiation , 2016, The Journal of Neuroscience.

[63]  Ashwin G Ramayya,et al.  A DTI investigation of neural substrates supporting tool use. , 2010, Cerebral cortex.

[64]  S. Holm A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[65]  J. Sharpe,et al.  Deficits of smooth‐pursuit eye movement after unilateral frontal lobe lesions , 1995, Annals of neurology.

[66]  David W. Franklin,et al.  Motor Effort Alters Changes of Mind in Sensorimotor Decision Making , 2014, PloS one.

[67]  Eli Brenner,et al.  Continuously updating one's predictions underlies successful interception. , 2018, Journal of neurophysiology.

[68]  J. Enns,et al.  On-line control of pointing is modified by unseen visual shapes , 2007, Consciousness and Cognition.

[69]  Karl R Gegenfurtner,et al.  Effects of contrast on smooth pursuit eye movements. , 2005, Journal of vision.

[70]  M. Sakagami,et al.  Functional role of the ventrolateral prefrontal cortex in decision making , 2007, Current Opinion in Neurobiology.

[71]  M. Goodale,et al.  An evolving view of duplex vision: separate but interacting cortical pathways for perception and action , 2004, Current Opinion in Neurobiology.

[72]  Leslie G. Ungerleider,et al.  A general mechanism for perceptual decision-making in the human brain , 2004, Nature.

[73]  P. Cisek,et al.  Modulation of Premotor and Primary Motor Cortical Activity during Volitional Adjustments of Speed-Accuracy Trade-Offs , 2016, The Journal of Neuroscience.

[74]  Daniel M Wolpert,et al.  Parallel specification of competing sensorimotor control policies for alternative action options , 2016, Nature Neuroscience.

[75]  Philippe Lefèvre,et al.  Overlap of movement planning and movement execution reduces reaction time by up to 100ms , 2016, bioRxiv.

[76]  Jason P Gallivan,et al.  The dorsal "action" pathway. , 2018, Handbook of clinical neurology.

[77]  A. Fuchs,et al.  Further properties of the human saccadic system: eye movements and correction saccades with and without visual fixation points. , 1969, Vision research.

[78]  Birk Diedenhofen,et al.  cocor: A Comprehensive Solution for the Statistical Comparison of Correlations , 2015, PloS one.

[79]  J. Gold,et al.  The neural basis of decision making. , 2007, Annual review of neuroscience.

[80]  R. Lencer,et al.  Neurophysiology and neuroanatomy of smooth pursuit in humans , 2008, Brain and Cognition.

[81]  Pratik K. Mutha,et al.  The influence of visual target information on the online control of movements , 2015, Vision Research.

[82]  A. Milner,et al.  How do the two visual streams interact with each other? , 2017, Experimental Brain Research.

[83]  T. Paus,et al.  Transcranial Magnetic Stimulation of Frontal Oculomotor Regions during Smooth Pursuit , 2006, The Journal of Neuroscience.

[84]  D. Robinson,et al.  The upper limit of human smooth pursuit velocity , 1985, Vision Research.

[85]  O. J. Dunn,et al.  Correlation Coefficients Measured on the Same Individuals , 1969 .

[86]  Sung Jun Joo,et al.  Decision-related perturbations of decision-irrelevant eye movements , 2016, Proceedings of the National Academy of Sciences.

[87]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[88]  D. Wolpert,et al.  A common mechanism underlies changes of mind about decisions and confidence , 2015, eLife.

[89]  Hugo Merchant,et al.  Behavioral and neurophysiological aspects of target interception. , 2009, Advances in experimental medicine and biology.

[90]  Matthew J. Crossley,et al.  Credit assignment in movement-dependent reinforcement learning , 2016, Proceedings of the National Academy of Sciences.

[91]  F. Lacquaniti,et al.  Visuo-motor coordination and internal models for object interception , 2009, Experimental Brain Research.