Spatiotemporal tuning of brain activity and force performance

The spatial and temporal features of visual stimuli are either processed independently or are conflated in specific cells of visual cortex. Although spatial and temporal features of visual stimuli influence motor performance, it remains unclear how spatiotemporal information is processed beyond visual cortex in brain regions that control movement. We used functional magnetic resonance imaging to examine how brain activity and force control are influenced by visual gain at a high visual feedback frequency of 6.4 Hz and a low visual feedback frequency of 0.4 Hz. At 6.4 Hz, increasing visual gain led to improved force performance and increased activity in classic areas of the visuomotor system-V5, IPL, SPL, PMv, SMA-proper, and M1. At 0.4 Hz, increasing gain also led to improved force performance. In addition to activation in M1/PMd and IPL in the visuomotor system, increasing visual gain at 0.4 Hz also corresponded with activity in the striatal-frontal circuit including DLPFC, ACC, and widespread activity in putamen, caudate, and SMA-proper. This study demonstrates that the frequency of visual feedback drives where in the brain visual gain mediated reductions in force error are regulated.

[1]  J. Perrone A Single Mechanism Can Explain the Speed Tuning Properties of MT and V1 Complex Neurons , 2006, The Journal of Neuroscience.

[2]  Pooja Wasson,et al.  Predicting grip force amplitude involves circuits in the anterior basal ganglia , 2010, NeuroImage.

[3]  R. J. Seitz,et al.  The role of V5 (hMT+) in visually guided hand movements: an fMRI study , 2004, The European journal of neuroscience.

[4]  R. Enoka,et al.  Steadiness is reduced and motor unit discharge is more variable in old adults , 2000, Muscle & nerve.

[5]  Janey Prodoehl,et al.  Basal ganglia mechanisms underlying precision grip force control , 2009, Neuroscience & Biobehavioral Reviews.

[6]  Paul Van Hecke,et al.  Internal vs external generation of movements: differential neural pathways involved in bimanual coordination performed in the presence or absence of augmented visual feedback , 2003, NeuroImage.

[7]  K. Newell,et al.  Intermittency in the control of continuous force production. , 2000, Journal of neurophysiology.

[8]  K. Newell,et al.  Noise, information transmission, and force variability. , 1999, Journal of experimental psychology. Human perception and performance.

[9]  Pamela S. Haibach,et al.  Visual angle is the critical variable mediating gain-related effects in manual control , 2006, Experimental Brain Research.

[10]  W. Newsome,et al.  Motion selectivity in macaque visual cortex. II. Spatiotemporal range of directional interactions in MT and V1. , 1986, Journal of neurophysiology.

[11]  Matthew B Spraker,et al.  Cortical and subcortical mechanisms for precisely controlled force generation and force relaxation. , 2009, Cerebral cortex.

[12]  M. Hallett,et al.  Mesial motor areas in self-initiated versus externally triggered movements examined with fMRI: effect of movement type and rate. , 1999, Journal of neurophysiology.

[13]  David E Vaillancourt,et al.  Selective regions of the visuomotor system are related to gain-induced changes in force error. , 2010, Journal of neurophysiology.

[14]  Takashi Hanakawa,et al.  Differential contribution of the supplementary motor area to stabilization of a procedural motor skill acquired through different practice schedules. , 2010, Cerebral cortex.

[15]  D. Vaillancourt,et al.  Neural Basis for the Processes That Underlie Visually-guided and Internally-guided Force Control in Humans , 2003 .

[16]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[17]  P. van Donkelaar,et al.  The Human Dorsal Premotor Cortex Generates On-Line Error Corrections during Sensorimotor Adaptation , 2006, The Journal of Neuroscience.

[18]  S. Funahashi,et al.  Working memory and prefrontal cortex , 1994, Neuroscience Research.

[19]  T. Ebner,et al.  What features of visually guided arm movements are encoded in the simple spike discharge of cerebellar Purkinje cells? , 1997, Progress in brain research.

[20]  G. Goldberg Supplementary motor area structure and function: Review and hypotheses , 1985, Behavioral and Brain Sciences.

[21]  Hong Yu,et al.  Region of interest template for the human basal ganglia: Comparing EPI and standardized space approaches , 2008, NeuroImage.

[22]  Rogier B. Mars,et al.  Dorsolateral Prefrontal Cortex, Working Memory, and Prospective Coding for Action , 2007, The Journal of Neuroscience.

[23]  R. Desimone,et al.  Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque , 1996, The Journal of Neuroscience.

[24]  P. Goldman-Rakic Cellular basis of working memory , 1995, Neuron.

[25]  Klaus-Peter Hoffmann,et al.  Temporal relation of population activity in visual areas MT/MST and in primary motor cortex during visually guided tracking movements. , 2002, Cerebral cortex.

[26]  R. Mansfield,et al.  Analysis of visual behavior , 1982 .

[27]  T. Ebner,et al.  Single trial coupling of Purkinje cell activity to speed and error signals during circular manual tracking , 2008, Experimental Brain Research.

[28]  William Gaetz,et al.  Activation of area MT/V5 and the right inferior parietal cortex during the discrimination of transient direction changes in translational motion. , 2007, Cerebral cortex.

[29]  Nicholas J. Priebe,et al.  Tuning for Spatiotemporal Frequency and Speed in Directionally Selective Neurons of Macaque Striate Cortex , 2006, The Journal of Neuroscience.

[30]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[31]  Chara Vakrou,et al.  Induced Deficits in Speed Perception by Transcranial Magnetic Stimulation of Human Cortical Areas V5/MT+ and V3A , 2008, The Journal of Neuroscience.

[32]  Stefan Everling,et al.  Task-relevant Output Signals are Sent from Monkey Dorsolateral Prefrontal Cortex to the Superior Colliculus during a Visuospatial Working Memory Task , 2009, Journal of Cognitive Neuroscience.

[33]  W. Jagust,et al.  Striatal dopamine and working memory. , 2009, Cerebral cortex.

[34]  K. Johnston,et al.  Monkey Dorsolateral Prefrontal Cortex Sends Task-Selective Signals Directly to the Superior Colliculus , 2006, The Journal of Neuroscience.

[35]  Semir Zeki,et al.  Motion processing, directional selectivity, and conscious visual perception in the human brain , 2008, Proceedings of the National Academy of Sciences.

[36]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[37]  Mary A. Mayka,et al.  Intermittent visuomotor processing in the human cerebellum, parietal cortex, and premotor cortex. , 2006, Journal of neurophysiology.

[38]  Daniel M. Corcos,et al.  Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: A meta-analysis , 2006, NeuroImage.

[39]  S. Bressler,et al.  Large-scale visuomotor integration in the cerebral cortex. , 2007, Cerebral cortex.

[40]  C. Pierrot-Deseilligny,et al.  Decisional role of the dorsolateral prefrontal cortex in ocular motor behaviour. , 2003, Brain : a journal of neurology.

[41]  P. Rossini,et al.  Lateralized contribution of prefrontal cortex in controlling task-irrelevant information during verbal and spatial working memory tasks: rTMS evidence , 2008, Neuropsychologia.

[42]  Alan C. Evans,et al.  MRI Atlas of the Human Cerebellum , 2000 .

[43]  S. Swinnen,et al.  Changes in brain activation during the acquisition of a new bimanual coordination task , 2004, Neuropsychologia.

[44]  Klaus-Peter Hoffmann,et al.  Influence of visually guided tracking arm movements on single cell activity in area MT , 2009, Experimental Brain Research.

[45]  J. Krakauer,et al.  Differential cortical and subcortical activations in learning rotations and gains for reaching: a PET study. , 2004, Journal of neurophysiology.

[46]  K R Thulborn,et al.  Visual feedback to stabilize head position for fMRI , 1999, Magnetic resonance in medicine.

[47]  Ivan Toni,et al.  Parieto-Frontal Connectivity during Visually Guided Grasping , 2007, The Journal of Neuroscience.

[48]  J. Patton,et al.  Evaluation of robotic training forces that either enhance or reduce error in chronic hemiparetic stroke survivors , 2005, Experimental Brain Research.

[49]  C. Pierrot-Deseilligny,et al.  The Role of the Human Dorsolateral Prefrontal Cortex in Ocular Motor Behavior , 2005, Annals of the New York Academy of Sciences.

[50]  A Berthoz,et al.  Visual perception of motion and 3-D structure from motion: an fMRI study. , 2000, Cerebral cortex.

[51]  Takashi Hanakawa,et al.  Functional coupling underlying motor and cognitive functions of the dorsal premotor cortex , 2009, Behavioural Brain Research.

[52]  Robin Laycock,et al.  Evidence for fast signals and later processing in human V1/V2 and V5/MT+: A TMS study of motion perception. , 2007, Journal of neurophysiology.

[53]  P. Goldman-Rakic,et al.  Modulation of Dorsolateral Prefrontal Delay Activity during Self-Organized Behavior , 2006, The Journal of Neuroscience.

[54]  Rachael D. Seidler,et al.  Contributions of Spatial Working Memory to Visuomotor Learning , 2010, Journal of Cognitive Neuroscience.

[55]  Nicholas J. Priebe,et al.  The Neural Representation of Speed in Macaque Area MT/V5 , 2003, The Journal of Neuroscience.

[56]  T. Sawaguchi,et al.  Prefrontal cortical representation of visuospatial working memory in monkeys examined by local inactivation with muscimol. , 2001, Journal of neurophysiology.

[57]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[58]  Leslie G. Ungerleider,et al.  Involvement of human left dorsolateral prefrontal cortex in perceptual decision making is independent of response modality , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[59]  S. Funahashi Prefrontal cortex and working memory processes , 2006, Neuroscience.

[60]  Rainer Goebel,et al.  The temporal characteristics of motion processing in hMT/V5+: Combining fMRI and neuronavigated TMS , 2006, NeuroImage.

[61]  D Le Bihan,et al.  The Dorsolateral Prefrontal Cortex (dlpfc) Plays a Key Role in Working Memory (wm). yet Its Precise Contribution , 2022 .

[62]  M. Inase,et al.  Neuronal activity in the primate premotor, supplementary, and precentral motor cortex during visually guided and internally determined sequential movements. , 1991, Journal of neurophysiology.

[63]  Peter A. Tass,et al.  Timing of V1/V2 and V5+ activations during coherent motion of dots: An MEG study , 2007, NeuroImage.