Name: methods to explore the influence of top-down visual processes on motor behavior
Uploaded: 2014-04-16T16:00:00
Description: Watch this Scientific Journal Video about Methods to Explore the Influence of Top-down Visual Processes on Motor Behavior at JoVE.com

The authors would like to acknowledge the members of the Laboratory of Vision Research and the Sensory-Motor Integration Laboratory for helping run participants in this study, Polina Yanovich, Joshua Dobias, and Robert W. Isenhower for help in the initial design phase, and Tom Grace for his help in building the stimulus. This work was supported by the following sources: the NSF Graduate Research Fellowship Program: Award #DGE-0937373, the NSF CyberEnabled Discovery and Innovation Type I (Idea): Grant #094158, and the Rutgers-UMDNJ NIH Biotechnology Training Program: Grant # 5T32GM008339-22.

1. Building the Stimulus Apparatus
<ol>
	<li>Construct a moveable platform on a sliding track. Each stimulus will be placed on the moveable platform depending on the type of trial called for.</li>
	<li>Secure the track onto a table at an appropriate height that allows for the stimulus platform to be at eye-level with the participant to be seated in front of the table.</li>
	<li>Attach a retractable spring mechanism to the stimulus platform. Connect the input to the spring mechanism to a circuit board.</li>
	<li>Place a...

<ol>
	<li>Schneider, G. E. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Two+visual+systems.">Two visual systems.</a> Science. 163, 895-902 (1969).</li><li>Ingle, D., Goodale, M. A., Mansfield, R. J. W. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=.">.</a> Analysis of visual behavior. , (1982).</li><li>Goodale, M. A., Milner, A. D. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Separate+visual+pathways+for+perception+and+action.">Separate visual pathways for perception and action.</a> Trends Neurosci. 15, 20-25 (1992).</li><li>James, T. W., Culham, J., Humphrey, G. K., Milner, A. D., Goodale, M. 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A. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Perceptual+illusion+and+the+real-time+control+of+action.">Perceptual illusion and the real-time control of action.</a> Spat. Vis. 16, 243-254 (2003).</li><li>Schenk, T. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Visuomotor+robustness+is+based+on+integration+not+segregation.">Visuomotor robustness is based on integration not segregation.</a> Vis. Res. 50, 2627-2632 (2010).</li><li>Schenk, T. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=No+dissociation+between+perception+and+action+in+patient+DF+when+haptic+feedback+is+withdrawn.">No dissociation between perception and action in patient DF when haptic feedback is withdrawn.</a> J. Neurosci. 32, 2013-2017 (2012).</li><li>Gegenfurtner, K., Henriques, D., Krauzlis, R. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Recent+advances+in+perception+and+action.">Recent advances in perception and action.</a> Vis. Res. 51, 801-803 (2011).</li><li>Binkofski, F., Buxbaum, L. J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Two+action+systems+in+the+human+brain.">Two action systems in the human brain.</a> Brain Lang. , (2012).</li><li>Aglioti, S., DeSouza, J. F., Goodale, M. A. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Size-contrast+illusions+deceive+the+eye+but+not+the+hand.">Size-contrast illusions deceive the eye but not the hand.</a> Curr. Biol. 5, 679-685 (1995).</li><li>Franz, V. H., Gegenfurtner, K. R., Bulthoff, H. H., Fahle, M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Grasping+visual+illusions:+no+evidence+for+a+dissociation+between+perception+and+action.">Grasping visual illusions: no evidence for a dissociation between perception and action.</a> Psychol. Sci. 11, 20-25 (2000).</li><li>Gilster, R., Kuhtz-Buschbeck, J. P., Wiesner, C. D., Ferstl, R. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Grasp+effects+of+the+Ebbinghaus+illusion+are+ambiguous.">Grasp effects of the Ebbinghaus illusion are ambiguous.</a> Exp. Brain Res. 171, 416-420 (2006).</li><li>Papathomas, T. V. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Art+pieces+that+'move'+in+our+minds+&#8211;+an+explanation+of+illusory+motion+based+on+depth+reversal.">Art pieces that 'move' in our minds &#8211; an explanation of illusory motion based on depth reversal.</a> Spatial Vis. 21, 79-95 (2007).</li><li>Papathomas, T. V., Bono, L. M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Experiments+with+a+hollow+mask+and+a+reverspective:+top-down+influences+in+the+inversion+effect+for+3-D+stimuli.">Experiments with a hollow mask and a reverspective: top-down influences in the inversion effect for 3-D stimuli.</a> Perception. 33, 1129-1138 (2004).</li><li>Hill, H., Johnston, A. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=The+hollow-face+illusion:+object-specific+knowledge,+general+assumptions+or+properties+of+the+stimulus.">The hollow-face illusion: object-specific knowledge, general assumptions or properties of the stimulus.</a> Perception. 36, 199-223 (2007).</li><li>Hartung, B., Schrater, P. R., Bulthoff, H. H., Kersten, D., Franz, V. H. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Is+prior+knowledge+of+object+geometry+used+in+visually+guided+reaching.">Is prior knowledge of object geometry used in visually guided reaching.</a> J. Vis. 5, 504-514 (2005).</li><li>Kroliczak, G., Heard, P., Goodale, M. A., Gregory, R. L. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Dissociation+of+perception+and+action+unmasked+by+the+hollow-face+illusion.">Dissociation of perception and action unmasked by the hollow-face illusion.</a> Brain Res. 1080, 9-16 (2006).</li><li>Torres, E. B. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Two+classes+of+movements+in+motor+control.">Two classes of movements in motor control.</a> Exp. Brain Res. 215, 269-283 (2011).</li><li>Torres, E. B. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Signatures+of+movement+variability+anticipate+hand+speed+according+to+levels+of+intent.">Signatures of movement variability anticipate hand speed according to levels of intent.</a> Behav. Brain Func. 9. 10, 10 (2013).</li><li>Torres, E. B., Heilman, K. M., Poizner, H. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Impaired+endogenously+evoked+automated+reaching+in+Parkinson's+disease.">Impaired endogenously evoked automated reaching in Parkinson's disease.</a> J. Neurosci. 31, 17848-17863 (2011).</li><li>Rencher, A. 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Our methods provide a platform to test the validity of perception-action models by analyzing the entire unfolding of movement in relation to the experimental task. The paradigm can be modified to test other types of visual stimuli to broaden this area of research. For example, other 3D DIIs can be tested on the apparatus to see how interactions between top-down and bottom-up processes translate to various stimuli. The methods can also be tailored to test clinical populations that may have perturbations in perception and ...

Vision-for-Perception vs. Vision-for-Action
In order to successfully navigate the environment, information from the visual system is utilized to help coordinate human movement. How visual information is selected and prioritized to influence motor actions remains unclear. Two major anatomical projections arise from the primary visual cortex to form the ventral ("what", or "vision for perception") pathway, extending to the temporal area, and the dorsal ("where", or "vision for action") pathway, to the parietal lobe1-2. The ventral stream is implicated in utilizing visual information for perceptual processes such as object recognition and identification, whereas the dorsal stream is thought to exclusively process signals for action guidance and spatial awareness. The question asked is whether or not top-down processes from the ventral stream shape the way in which movements are executed.
The famous case study of Patient DF, evaluated by Goodale and Milner in 1992, provided strong evidence and support for the visual two-streams hypothesis, which claims that ventral and dorsal stream processes are separable for perception and action3. In theory, bottom-up signals of motion parallax and binocular disparity can override top-down perceptual information such as prior knowledge and familiarity in order to accurately guide our actions, suggesting that motor planning is impervious to ventral stream control. DF, who suffered from visual form agnosia caused by bilateral ventral occipital lesions, retained accurate grasping ability towards objects that she had difficulty recognizing, supporting the premise of the visual two-streams hypothesis3-4. Because of case studies like DF, it was assumed that the functional ventral-dorsal stream dichotomy also existed in healthy, nonpathological individuals. However, whether or not these findings provide evidence for an absolute division of labor for perception and action in neurotypical populations has been hotly debated over the past twenty years5-10.
The Use of Illusions to Segregate Perception and Action
To test the visual two-streams hypothesis in neurotypical subjects, researchers employ visual illusions to investigate how skewed perceptual judgments of the environment affect our motor actions. The Ebbinghaus/Titchener Illusion, for example, uses a disk target surrounded by smaller disks that appears to be larger than another disk of the same size surrounded by larger circles; this is due to a size-contrast effect11. When participants reach to grasp the disk target, if the two-streams hypothesis holds true, then the grip aperture of the hand grabbing at the disk target would be unaffected by the illusion, causing the participant to act on the true geometry of the disk target rather than rely on incorrect perceptual size estimates. Aglioti et al. in fact report this behavior, reasoning that separate visual processes govern skilled actions and conscious perception11. Conversely, other groups have contested these results, finding no dissociation between perception and action processes when carefully controlling the matching of perceptual and grasping tasks, proposing an integration of visual stream information rather than a separation12. Despite several follow-up studies conducted to validate or refute the visual two-streams hypothesis using the Ebbinghaus Illusion, there are competing pieces of evidence to support both sides of the argument13.
To further explore the influence of visual perception on action processes, 3D depth inversion illusions (DII) have also been utilized. DIIs produce illusory motion and perceived depth reversal of scenes in which physically concave angles are perceived as convex and vice versa14. The Hollow Face Illusion is an example of a DII that generates the perception of a normal, convex face although the stimulus is physically concave, implicating the role of top-down influences such as prior knowledge and convexity bias to elicit the illusory percept15-16. Despite efforts to characterize motor behavior in reaching towards targets on the Hollow Face Illusion, evidence remains equivocal: one study reports an effect on motor output17 while another does not18. These studies rely on comparing perceptual depth estimates to endpoint distance calculations of the hand relative to targets located on the Hollow Face Illusion. Conflicting results on actions performed on this type of stimuli may be a result of the variations in methods used by researchers. Because the way in which ventral and dorsal stream information is utilized is still up to debate, this controversy sparks the need for a more robust stimulus with additional advanced measures of motor behavior.
This is precisely why a technique was developed using reverse-perspective stimuli, commonly referred to as "reverspectives", which form another class of DIIs14. Linear perspective cues that are painted on piecewise 3D planar surfaces produce competition between the physical geometry of the stimulus and the actual painted scene. Data-driven sensory signals, such as binocular disparity and motion parallax favor the veridical percept of the physical geometry, whereas experience-based familiarity with perspective favors the depth-inversion percept (Figure 1). The advantage of the reverspective is that it allows for the placement of a target on a stimulus surface whose perceived spatial orientation under the illusion differs by nearly 90 degrees from its physical orientation (Figures 1e and 1f). This huge difference greatly facilitates testing whether reach-for-grasping movements are or are not influenced by the illusion. This notion is key to exploring whether or not motor actions performed on the reverspective are affected by top-down influences from the ventral stream.
Movement Classes in Perception-Action Models
If different motor strategies are employed under illusory and veridical percepts when grabbing towards a target on a reverspective stimulus, then it can be easily tracked by studying the curvature of the hand&#39;s approach. Moreover, an analysis of the entire unfolding movement from initiation of the goal-directed movement to the spontaneous, automatic retraction of the hand back to its resting state may in fact bypass any shortcomings found in past methods of testing for perceptual influence on motor output. Recent studies highlight the significance of studying the balance between these two movement classes as well as the use of the spontaneous segments by the nervous systems for predictive and anticipatory control19-21,23-24. The newly statistically defined class of spontaneous-automatic movements provides new metrics and features that turn out to be as crucial as the goal-directed ones have been thus far to track sensory-motor changes and to quantify subtle aspects of natural behaviors.
To our knowledge, existing research on the visual two-streams hypothesis only focuses on goal-directed acts, thereby ignoring any effects on automatic transitional movements that are significant components to completing the visuomotor action loop. Emphasis therefore must be placed on the importance of automatic motions in order to fully capture both modes of motor behavior in the present paradigm to clarify issues concerning visual perception-action models. Here methods are developed to investigate the role of top-down signaling in the visual ventral stream on modulating motor behavior in the deliberate, goal-directed action domain in conjunction with spontaneous, transitional movements using a robust DII reverse-perspective stimulus.
Rationale
It is hypothesized that, if top-down visual processes influence the sensory-motor system, full movement trajectories toward the embedded target in the 3D reverse-perspective scene under the illusory percept will differ from the target approach elicited by the veridical percept (Figures 1e and 1f). Moreover, since the illusory percept of the reverspective stimulus is very similar to that obtained by a proper ("forced") perspective stimulus, reaches performed toward an embedded target on a reverspective should therefore be similar in characteristics to reaches conducted under the influence of the illusion on the reverspective stimulus (Figures 1c and 1f).
If top-down visual influences do not impact the movement trajectory, then it is hypothesized that reaches made under the illusory percept would exhibit the same characteristics as reaches made under the veridical percept on the reverspective stimulus (Figure 1e). In other words, both illusory and veridical percept reaches would be similar in nature, such that both forward trajectory paths would act on the true geometry of the stimulus. How effects observed in the forward reach translate in the automatic retraction of the hand is unknown. By employing a full motor analysis, we aim to advance our understanding of action and perception loops to clarify the existing issues at hand.

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			<td height="21" style="height:21px;width:276px;">Laboratory bench</td>
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			<td height="21" style="height:21px;width:276px;">Arduino</td>
			<td style="width:252px;">Smart Projects, Italy</td>
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			<td height="42" style="height:42px;width:276px;">MATLAB</td>
			<td style="width:252px;">The MathWorks Inc., Natick, MA, USA</td>
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			<td height="21" style="height:21px;width:276px;">Randot-dot Stereo Test</td>
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			<td height="21" style="height:21px;width:276px;">Proper-Perspective Stimulus</td>
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			<td height="21" style="height:21px;width:276px;">Polhemus Motion Capture System</td>
			<td style="width:252px;">Liberty, Colchester, VT, USA</td>
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			<td height="42" style="height:42px;width:276px;">The Motion Monitor Motion-Tracking Software</td>
			<td style="width:252px;">Innovative Sports Training, Inc., Chicago, IL</td>
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methods to explore the influence of top-down visual processes on motor behavior

Kinesthetic awareness is important to successfully navigate the environment. When we interact with our daily surroundings, some aspects of movement are deliberately planned, while others spontaneously occur below conscious awareness. The deliberate component of this dichotomy has been studied extensively in several contexts, while the spontaneous component remains largely under-explored. Moreover, how perceptual processes modulate these movement classes is still unclear. In particular, a currently debated issue is whether the visuomotor system is governed by the spatial percept produced by a visual illusion or whether it is not affected by the illusion and is governed instead by the veridical percept. Bistable percepts such as 3D depth inversion illusions (DIIs) provide an excellent context to study such interactions and balance, particularly when used in combination with reach-to-grasp movements. In this study, a methodology is developed that uses a DII to clarify the role of top-down processes on motor action, particularly exploring how reaches toward a target on a DII are affected in both deliberate and spontaneous movement domains.

1. Hand Path Trajectories
Results are shown for Representative Subject VT. The Wilk&#39;s Lambda Test Statistic allows for the reduction of our three-dimensional space data into a scalar value by the use of determinants. The Wilk&#39;s lambda statistic uses the likelihood ratio test <img alt="" fo:content-width=".8in" src="/files/ftp_upload/51422/51422eq1.jpg" width="90" />, in which the &#39;within&#39; sum of squares and products form matrix E, and the &#39;total&#39; sum of squares and product...

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Methods to Explore the Influence of Top-down Visual Processes on Motor Behavior

It is unclear how top-down signals from the ventral visual stream affect movement. We developed a paradigm to test motor behavior towards a target on a 3D depth inversion illusion. Significant differences are reported in both deliberate, goal-directed movements and automatic actions under illusory and veridical viewing conditions.

Kinesthetic awareness is important to successfully navigate the environment. When we interact with our daily surroundings, some aspects of movement are ...

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Integrating Visual Psychophysical Assays within a Y-Maze to Isolate the Role that Visual Features Play in Navigational Decisions

Collective animal behavior arises from individual motivations and social interactions that are critical for individual fitness. Fish have long inspired ...

Using the Race Model Inequality to Quantify Behavioral Multisensory Integration Effects

Multisensory integration research investigates how the brain processes simultaneous sensory information. Research on animals (mainly cats and primates) ...

Exploring Infant Sensitivity to Visual Language using Eye Tracking and the Preferential Looking Paradigm

We discuss the use of the preferential looking paradigm in eye tracking studies in order to study how infants develop, understand, and attend to the world ...

Investigating the Effect of Visual Imagery and Learning Shape-Audio Regularities on Bouba and Kiki

This article presents a protocol for investigating the role of visual imagery in the bouba/kiki-effect, whether training in noticing the bouba/kiki ...