Cahiers de Psychologic Cognitive/ Current Psychology of Cognition 2002, 21 (4-5), 343-375 Short-term adaptive control processes in vergence eye movement John L. Semmlow,1'2 Weihong Yuan,2 and Tara 3 Alvarez 1. UMDNJ, New Brunswick, NJ, USA 2. Rutgers University, Piscataway, NJ, USA 3. New Jersey Institute of Technology, Newark, NJ, USA Abstract The "Dual Mode" theory for the control of disparity vergence eye movements states that two control components, a preprogrammed "transient" component and a feedback control "sustained component, mediate the motor response. Although prior experimental work has isolated and studied the transient component, little is known of the contribution of the sustained component to vergence response. The timing between the two components and their relative magnitudes are of interest as they have implications on the control strategies used to coordinate the two components. Modeling studies can provide an estimate of component magnitudes, but cannot uniquely identify the component timing. The work presented in this paper applies Principal Component Analysis (PCA) to ensemble data both to confirm the presence of two major components and for data reduction. A novel, ensemble version of Independent Component Analysis (1CA), is then exploited to estimate the contribution of the two control components to the eye movement. Other recent experiments have shown that the vergence system is capable of rapidly modifying its dynamic characteristics (short-term adaptation) when exposed to specially designed "adapting" stimuli. Adapted Correspondence should be sent to Department of Surgery (Bioengineering), Robert Wood Johnson Medical School - UMDNJ, New Brunswick, NJ 08903, USA (email: [email protected]) 344 J. L.Semmlow et al. responses were characterized by faster dynamics often featuring large overshoots. ICA analysis of adapted and normal responses show that the enhanced dynamics of adapted responses are due to an increase in transient component amplitude. In addition, the sustained component of adapted responses often showed double-step behavior in the later portion of the response. Finally, the extent of adaptation produced appeared to be related to the unadapted transient component amplitude. Key words: eye movements, disparity vergence response, independent component analysis, vergence components. INTRODUCTION The complex strategies used by the brain to implement eye movement behavior have evolved in the nervous system to solve a difficult control problem: the need to produce fast and highly accurate responses in the face of substantial computational delays. One of the most dramatic of these strategies is the lavish use of independent neural control centers to mediate various oculomotor tasks. The major motor centers that are thought to support the control of eye movements are represented schematically in Figure 1. Note that the centers shown in Figure 1 represent only the motor side of the visuomotor system: complex tasks such as target identification and spatial localization would be mediated by different centers that are simply lumped together in Figure 1 under the heading "Stimulus Influences". This organization is a synthesis of extensive eye movement research in many laboratories involving both behavioral and neurophysiological approaches. The neural structures and their organization were originally inferred from behavioral data, but many have since been identified or confirmed in neurophysiological studies (shown as shaded). As shown, the centers can be divided into two broad categories: those that mediate version (tandem) movements and those that mediate vergence (opposition) movements. Although the version and vergence subsystems mediate different behaviors, and have different levels of performance, these is some structural similarity between them. The two subsystems are composed of a high speed and low speed component, with the low speed component under the influence of visual feedback. In addition, each subsystem receives a contribution from processes that are driven by stimuli other Adaptive control in vergence eye movement 345 than the retinal image position: the version subsystem receives a signal from the vestibular apparatus that is sensitive to head movement while the vergence sub-system receives an input from accommodative processes that is related to blur. Accommodative Prediction ( Vergence Adaptation ( )•• '" * Prediction ( Adaptation Figure 1. Schematic representation of the major motor centers active in the control of eye movements. For simplicity, feedback pathways are not explicitly shown, but the "Stimulus Influences" of both smooth pursuit and slow vergence are modified by visual feedback. Shaded neural centers and their associated pathways have been con- firmed in neurological studies. Dashed lines indicate pathways not yet experi- mentally verified or controversial. The control of version eye movements has received much attention, particularly the saccadic and smooth pursuit components. The appeal of these two systems is likely due to the extraordinary performance of the saccadic system. Saccadic movements appear to be time-optimal (Bahill & Stark, 1979; Robinson, 1975) and can reach velocities of nearly a 1,000 deg/sec (Bahill, Clark, & Stark, 1975). Prediction is known to occur in both the saccadic and smooth pursuit systems (Young, 1971; 346 /. L.Semmlow et al. Stark 1971). In the former, prediction is observed as a marked decrease in the response latency of a saccadic response (Young, 1971), while in the latter, prediction improves the tracking performance (Stark, 1971; Robinson, Gordon, & Gordon, 1986). Prediction can be activated simply by using target motions that are predictable. If the timing of the stimulus is regular, such as a square wave stimulus pattern, prediction in the saccadic system will reduce the saccadic response latency, normally around 200 msec, to near zero (Stark, 1971). Similarly, if the stimulus trajectory follows a simple periodic function, such as a sine wave, the smooth tracking error decreases substantially (Young, 1971; Stark, 1971). The saccadic system is also influenced by both long-term and short-term adaptive processes (McLaughlin, 1967; Semmlow, Gauthier, & Vercher, 1989; Optican & Miles, 1985; Optican, Zee, & Chu, 1985). Smooth pursuit adaptive processes are also known to exist (Optican et al., 1985), but have not been extensively studied. Short-term saccadic adaptation can be evoked experimentally using training stimuli that force post-saccadic errors (McLaughlin, 1967; Semmlow et al., 1989), but this protocol requires a large number of adaptive training saccades. Since both saccadic and smooth pursuit systems mediate only version eye movements, they cannot be used to change the depth of the eye fixation point. This task is relegated to the vergence motor control system which drives the two eyes in opposition. The vergence system receives information on both the "disparity" of the retinal image of interest (the difference in the position of the two retinal target images with respect to a set of corresponding retinal reference positions), and the blur of the target image. Image blur comes from an error in the focusing of the lens and is related to target distance. Blur-induced vergence (termed "accommodative vergence") may play a role in maintaining vergence position, but has been shown to be too slow to contribute significantly to the dynamic vergence response (Hung, Semmlow, & Ciuffreda, 1983). The vergence system shares some of the same features as found in the saccadic system. For example, closely-spaced step-like responses have been observed in response to single step stimuli in both saccades and vergence as discussed below. Vergence control processes also include a prediction operator, and the behavior of prediction in vergence is quite similar to that seen in saccades: prediction reduces latency and improves smooth tracking (Yuan, Semmlow, & Munoz, 1998, 2000). Another paper in this series (Alvarez, Semmlow, Yuan, & Munoz, 2002) ad- dresses the behavior of prediction in vergence eye movements. Vergence Adaptive control in vergence eye movement 347 moments also respond adaptively to certain stimulus conditions. In fact, adaptive changes in vergence produced by special adaptive stimuli are both faster and more dramatic than those produced in saccades. Vergence control concepts Abnormalities in the control of disparity vergence eye movements underlie many binocular clinical conditions such as strabismus (Schor & Ciuffreda, 1983), yet the basic neural control strategy which guides these movements is only just beginning to be revealed. Though scientific interest in disjunctive eye movements can be 'traced to the early 19th century, it was not until 1961 that Rashbass and Westheimer (1961) pre- sented a quantitative theory for the neural control of these movements. The movements produced by the vergence control system are not as dynamically exciting as those produced by the saccadic system, reaching peak velocities only one quarter of that of saccades (Hung, Ciuffreda, Semmlow, & Horng, 1994). That behavior, coupled with the very low position errors achieved by this system (sustained binocular position errors are only several minutes of arc), has led control oriented re- searchers to conclude that vergence responses are under the guidance of a single feedback control system (Rashbass & Westheimer, 1961; Zuber & Stark, 1968; Krishnan & Stark, 1977). Subsequent support was provided by experimental (Zuber & Stark, 1968) and analytical