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

Podsumowanie

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.

Streszczenie

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.

Wprowadzenie

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 lobe^1-2. 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 hypothesis^3-4. 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 years^5-10.

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 percept^15-16. 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'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 control^19-21,23-24. 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.

Access restricted. Please log in or start a trial to view this content.

Protokół

1. Building the Stimulus Apparatus

1. 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.
2. 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.
3. Attach a retractable spring mechanism to the stimulus platform. Connect the input to the spring mechanism to a circuit board.
4. Place a set of lamps behind the participant's seat, facing the stimulus platform. It is important to illuminate the stimulus platform evenly because uneven lighting may cast shadows that interfere with the illusory percept. Connect the set of lamps to a converter that links it to the circuit board.
5. Attach a switch box to the edge of the table closest to the where the participant will be seated. Participants place their hand on the switch box at the beginning of each trial and activate the switch as soon as they lift their hand to execute the reach movement. Link the switch box input to the circuit board.
6. Connect each output pin of the circuit board to a pin on the microcontroller to control the simultaneous activation of the retraction of the moving platform via the spring mechanism and the turning off of lights once the switch box is triggered. The stimulus must retract and the lights must turn off after the initiation of the reach movement in each trial to prevent any online visual corrections and haptic feedback from occurring. The switch box is employed so that the stimulus retraction and darkness onset are performed only after movement begins, making this an immediate reach task.
7. Write a MATLAB program that controls the microcontroller signals. Use the MATLAB code to store a sequence of trials and instruct the experimenter what stimuli and viewing conditions to use for each trial.
8. Construct training stimuli, the reverse-perspective stimulus, and the proper-perspective stimulus (Figures 1 and 2). Training stimuli consist of two rectangular panels representing the isolated right surface wall of the middle building embedded in the reverse-perspective stimulus and the proper-perspective stimulus. The purpose of the training stimuli will be discussed in the experimental procedure. Affix red planar disk targets to the right of the midline of the stimuli.

2. Participants

1. Obtain written informed consent of the IRB approved protocol in compliance with the Declaration of Helsinki before beginning the experimental session.
2. Test the participant for visual acuity in each eye, stereopsis (using a Randot-Stereo Test), and eye dominance.
3. Set-up the motion capture system. Use fourteen electro-magnetic sensors at 240 Hz and motion-tracking software. The high-resolution recording system allows for the in-depth analysis of the unfolding of movement in three dimensions of fourteen sensors simultaneously, that past studies lack.
   1. Place twelve of the fourteen sensors on the following body segments using sports bands designed to optimize unrestricted movement of the body: head, trunk, right and left shoulders, left upper arm, left forearm, left wrist, right upper arm, right forearm, right wrist, right hand index finger, and right hand thumb.
   2. Place the remaining two sensors on the backside of the stimuli directly behind the target location to attain an accurate position of the target in 3D space relative to the participant during the training and experimental blocks.

3. Experimental Procedure

1. Place all stimuli out of view from the participant at this time. Turn off all lights except for the lamps used to illuminate the stimulus platform. Dim any computer screens that are in use to run the experiment so that their lights do not interfere with the even lighting projected onto the apparatus.
2. Before beginning any trials, inform the participant of the experiment flow. Notify them of the stimulus retraction and turning off of lights once they initiate movement by lifting their hand off the switch box. Remind them not to try to follow the retracting platform, but to only grab at where the target was last seen. Demonstrate how to grab at where they last remember seeing the target by approaching it normal to the perceived surface.
3. Begin practice trials. These trials allow for the participant to become comfortable with the setup. There is no test stimulus on the platform - only a black board with a center pole protrusion used to attach stimuli. Instruct the participant to reach at the center pole and to bring the hand back to rest upon completing the reach, at his/her own pace; repeat for three trials. Note: It is important not to give instructions on how to retract the hand; this component should be automatic and below conscious control.
4. Initiate training trials. Ask the participant to close his/her eyes after each trial for the remainder of the experiment. While the participant's eyes are closed, affix the training stimulus called for in the MATLAB program to the center pole; the order of training stimulus presentation is randomized by the MATLAB program for a total of eight trials, four for each stimulus. Training stimuli help demonstrate the curvature of the reach when asked to grab at targets on physical surfaces representative of the targets used in the experimental stimuli.
5. Begin experimental trials. There are three stimulus conditions for the experimental trials: (1) reverspective under illusory percept, as in Figure 1f (REV-ILLU), (2) reverspective under veridical percept, as in Figure 1e (REV-VER), and (3) proper-perspective (PRO), as in Figure 1c. Recall that conditions (1) and (2) utilize the same physical reverspective stimulus.
   1. First present the reverspective stimulus. Ask the participant if he/she can stabilize the illusory percept of the middle building "popping out" towards him/her. If the participant has trouble stabilizing the illusory percept, place a de-focusing lens on the nondominant eye to weaken stereopsis in order to preserve the illusory percept while maintaining reaching distance to the target¹⁸. If the participant requires the de-focusing lens, then make sure to instruct him/her to put them on before each REV-ILLU trial.
   2. After the first REV-ILLU trial, the MATLAB program will randomize the order of trials. For each trial, give the following instructions depending on the stimulus condition:
      REV-ILLU: "View the middle building as popping out towards you."
      REV-VER: "View the middle building as caving in away from you."
      PRO: "View the middle building as popping out towards you."
      Once the participant confirms a stable percept, ask them to grab at the target. Perform twelve trials for each condition for a total of 36 experimental trials.

4. Data Analysis

1. To analyze the movements in terms of the goal-directed reach and automatic retractions, first decompose the data into two movement classes by detecting the point at which the velocity of the movement, after its initiation, nears instantaneous zero velocity.
2. To look for differences in the curvature of hand path trajectories for each stimulus condition, perform the Wilk's Lambda Test Statistic on the 3-dimensional dataset at each point in time during the trajectory. The Wilk's Lambda Test reduces the likelihood test statistic Λ to a scalar value by way of determinants to help us deduce whether or not the mean trajectory vector for REV-ILLU is similar to REV-VER or PRO²².
3. To study the orientation of the hand towards the target at the end of the goal-directed reach, compare the angle formed between the unit approach vector generated by the thumb, index, and wrist sensor positions relative to the target's unit vector normal to the surface (Figures 5a and 5b).

Access restricted. Please log in or start a trial to view this content.

Wyniki

1. Hand Path Trajectories

Results are shown for Representative Subject VT. The Wilk'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's lambda statistic uses the likelihood ratio test , in which the 'within' sum of squares and products form matrix E, and the 'total' sum of squares and product...

Access restricted. Please log in or start a trial to view this content.

Dyskusje

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 ...

Access restricted. Please log in or start a trial to view this content.

Materiały

Name	Company	Catalog Number	Comments
Laboratory bench
Slidable Track with Retractable Spring			built in-house
Retractable Spring
Adjustable Lamps
Switch Box
Circuit Board
Arduino	Smart Projects, Italy
MATLAB	The MathWorks Inc., Natick, MA, USA
Randot-dot Stereo Test
Reverse-Perspective Stimulus			built in-house
Proper-Perspective Stimulus			built in-house
Training Stimuli			built in-house
Polhemus Motion Capture System	Liberty, Colchester, VT, USA
The Motion Monitor Motion-Tracking Software	Innovative Sports Training, Inc., Chicago, IL
Sport Sweatbands
De-Focusing Lens