Neural Processing in Vergence Eye Movements: A Time Based Study

Neural Processing in Vergence Eye Movements: A Time Based Study Tara L. Alvarez1 and John L. Semmlow1'2 Department of Biomedical Engineering, Rutgers University1, Department of Surgery, Bioengineering, Robert Wood Johnson, Medical School - UMDNJ2 New Brunswick, NJ Abstract Inward turning of the two eyes, termed disparity vergence, sometimes exhibits two closely-spaced, fast dynamic movements. These response doubles can provide information on the neural processes that control the fast, dynamic response. The second component of this pair could be generated by either an internal process or by external error from visual feedback. To differentiate between these two mechanisms, a comparison was made between doubles induced experimentally (using a "forced-error" protocol) and those that occur naturally in standard step responses. The two stimulus conditions produced response doubles with different timing properties. Since the forced-error doubles were generated by visual feedback, differences in timing imply that normally occurring double responses are mediated by an internal mechanism. This internal feedback mechanism is likely to be involved in the production and control of the fast dynamic portion of all vergence eye movements. INTRODUCTION To gain insight into how the brain produces the precise motor control seen in human eye movements, it is essential to extract as much information as possible from the behavior. This study will focus on the highly accurate vergence eye movement system that mediates inward or outward turning of the eyes and produces position accuracies within a fraction of a degree. While the vergence eye movement system normally responds to step stimuli with a single high-velocity response, occasionally, two high-velocity movements are seen. Experimental data has shown that these double responses occur when the first component has reduced amplitude, so that the movement would have fallen far short of that required by the stimulus. To produce the secondary response, the brain may either recompute the motor control signal based on an internal calculation of residual error or it may rely on visual feedback. In the former case, the motor control signal generated 0-7803-3848-0/97/$10.00 ©1997 IEEE

by the vergence neural center would be monitored internally, and an inadequate signal would trigger that center to produce a second response. In the latter case, feedback monitoring of the ongoing motor movement would show the inadequacy of the response which would trigger a second effort. To distinguish between these two possible mechanisms, a specially developed stimulus artificially generated vergence doubles using a forced-error protocol. These visually induced doubles were then compared with doubles occasionally seen in response to standard step stimuli. Since the forced-error doubles were produced by external visual information, a favorable comparison would indicate that normally occurring doubles were driven by external feedback. Conversely, differences in the two responses would indicate that an internal process generates the secondary response. METHODS The stimulus target consisted of a stereoscopic pair of vertical lines displayed on a pair of oscilloscopes viewed through mirrors. The stimuli were 8 deg standard steps and 4 deg forced-error steps. The forced-error protocol continually adjusted the stimulus target so that the effectiveness of the eye movement appeared to be reduced. As the eyes responded to an initial stimulus, the stimulus was proportionally increased to offset a portion of the movement. This would appear to the visual system as if the control system was always underestimating the signal needed to produce the desired movement. The eye movements were recorded using a commercially available limbus tracking device, the Skalar infrared eye movement monitor, which has a linear range of ±25 deg and a resolution of 1.5 min of arc. The stimulus construction and presentation as well as data acquisition were under computer control. Calibration points were recorded with each movement and used for off-line analysis. The data were analyzed using Matlab. Four subjects participated in the study.

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RESULTS The crux of this research was to determine if double high-velocity movements in response to standard step stimuli were initiated based on internal or external information. Figure 1 is a representative time plot of a double response from a standard 8 deg step stimulus and from a 4 deg forced-error stimulus. Both show secondary movements, but qualitative inspection shows that the two responses occur at different times and with different dynamics. This behavior was seen in all four subjects studied. Forced Error

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Figure 1: Typical time plots of standard step and forced-error response from Subj JS Figure 2 quantifies these differences by plotting the time at which the maximum velocity occurs relative to movement onset as a function of maximum velocity for both components. The solid symbols represent the primary response components; whereas, the open symbols are for the secondary components. Forced Error

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Figure 2: Timing Characteristics of Primary and Secondary Components from Subject JS Closed symbols: primary component Open symbols: secondary component These results are representative of all four subjects studied. There are two important features shown in

this figure. First, the time at which the primary component reaches maximum velocity is approximately the same for both stimuli. Second, the secondary component reaches maximum velocity earlier in standard step doubles. DISCUSSION The primary components from both types of responses exhibited the same timing characteristics. This demonstrates that both responses initially start off with the same neural processing strategy. The difference between the two responses is in the timing of the secondary component. The doubles produced by forced-error stimuli were driven by an external visual signal. In these movements, a feedback process must first sample the visual stimulus, determine that the ongoing movement was inadequate, then trigger a second fast component to aid the ongoing response. This process would take longer than a scheme based solely on an internal monitoring of the control signal. If internal monitoring showed that the initial neural signal was not large enough to successfully drive the eyes to the designated target, then a second signal could be triggered. This process should respond faster because it would bypass delays in the visual system. The response doubles to standard steps showed faster processing than externally driven forced-error doubles, implying an internal mechanism was used to generate naturally occurring doubles. The forced-error stimulus protocol is a powerful tool to study neural processing in vergence eye movements. The comparison between forced-error and normally occurring doubles indicates the existence of an internal process that monitors the initial control signal and has the capability of producing secondary signals. The existence of such an internal monitoring process suggests that a "local feedback" (Robinson et al. 1975) structure may be involved in the control of vergence eye movements, not only in monitoring the motor signal, but in its production as well.

REFERENCES Alvarez, TL, Semmlow, JL, Yuan, W. (1997). Submitted. Bridgeman, B. (1995) Ann. ofBME., 23, 409-422. Robinson, DA, Gordon, JL, Gordon, SE. (1975) Basic Mech. of Ocular Motility and Their Clinical Implications. Oxford. UK: Pergamon , 337-374. Semmlow, JL, Hung, GK, Horng, JL, Ciuffreda, KJ. (1994) Vision Research., 34, 1335-1343. 80