In the present study, we approach this question by analyzing the latency of combined eye movements. The rationale is the following: As explained in the Methods section, from the individual eye position signals, we derived two signals—the conjugate signal and the disconjugate signal—which could be produced by two interacting, but distinct oculomotor subsystems: the saccade and the vergence systems. Evidence for asynchrony in the initiation of the two components argues in favor of such a theoretical framework.
Most important, comparison between children and adults could help in the understanding of the role of learning and experience in the ability to synchronize multiple motor commands. Three different types of initiation were observed: the vergence component started first Fig. Figure 8 shows the percentage of each of these three types of initiation in children A and adults B. The other two patterns of initiation occurred less frequently. Inspection of the individual adult results in Fig. Thus, the adult results are idiosyncratic.
Some subjects started their combined movements predominately by triggering the saccade first, and others by triggering the two components together. To examine developmental aspects, we regrouped the 15 children into three groups, 4. Figure 9 presents the mean latency for each age group of children for pure A and combined B eye movements. It is evident that the latency of all eye movements decreased with age.
Figure 9C shows the mean percentage of different types of initiation of the combined movements, also as a function of age. Planned comparison of the percentage of simultaneous starting at the age of 4. In summary, all latencies decreased with age and approached adult levels at the ages of 10 to 12 years. In contrast, the way children initiated combined movements changed little with age, and their behavior remained different from that of adults, even at the age of 10 to 12 years.
The main findings can be summarized follows: All latencies and their variability of eye movements in 3-D space were longer in children than in adults, and there was a progressive decrease with age. Latencies approached or reached adult lengths at approximately 10 to 12 years. There were differences between latencies in different types of eye movements, both in children and adults. Differences in latency suggest that the visuomotor spatial and attentional processes involved e.
The presumably distinct triggering eye movement mechanisms matured with age, progressively and in parallel. A fundamental difference between children and adults resided in the capability of synchronization of the two components of combined movements. In children, most of the combined movements showed asynchrony i. Asynchrony was present at all ages studied, and, presumably, synchrony of movement reached adult levels beyond the age of 12 years.
Next, we will discuss in more detail each of these findings and their physiological significance. Latencies of pure saccades and pure vergence were longer in children than in adults. Our results for saccades are in agreement with prior studies. Thus, our study extends prior reports of long latency in children, even for saccades in more natural conditions.
As mentioned, saccade latency reflects several visuomotor and attentional processes that involves activation of a large neural circuitry from the retina to visual cortex, parietal cortex, frontal lobe, and superior colliculus and then to brain stem and extraocular muscles. The longer saccade latency has been attributed frequently to underdeveloped related cortex, and some investigations also have suggested that increased latency of saccades is related to difficulty in controlling visual fixation.
Our observations of increased latency of saccades in children and progressive decrease with age are compatible with the idea of progressive maturation, especially of the frontal lobe. Studies of latency in vergence in children are, to our knowledge, nonexistent. Latencies in vergence in the children in our study were also longer than in adults, and they decreased with age. The explanation for the length of latency in vergence could be similar to that for latency in saccades.
Indeed, it is likely that the triggering of saccade and vergence activates similar cortical circuitry and visuospatial and attentional processes. Note that the cortical circuitry controlling vergence is not well known in humans. There is, however, some evidence from animal studies for the involvement of the posterior parietal cortex PPC; see Mays and Gamlin 25 and frontal lobe see Gamlin and Yoon Moreover, Hasebe et al. The mean difference was approximately 15 ms and was statistically significant. In adults, we observed shorter latency of vergence than saccades in a few subjects only.
This result indicated that the difference in latency between saccade and vergence becomes subject dependent at the adult stage. For both children and adults, latency in saccades at close viewing distance was shorter by approximately 20 ms than that at far viewing distance. This observation is, to our knowledge, new. The origin of this difference could be sensory, oculomotor, attentional or any combination of these factors. This is compatible with electroencephalogram studies that also show dependence of latency in visual evoked potentials VEP on spatial frequency see Mihaylova et al.
It is also compatible with the study by Raymond, 31 showing that the reaction time to detect the change of a small letter of constant size was shortest at an individually determined close optical distance and that the time lengthened with the increase in viewing distance. Oculomotor reasons could include facilitation of disengagement of oculomotor fixation when the eyes are at high degree of convergence, such as is needed to fixate the close LED located at a cm viewing distance.
Finally, attentional reasons could include facilitation of disengagement of visual attention when the eyes converge at close. In the adult group, the results showed significantly longer latency for convergence than divergence the mean difference was approximately 20 ms. This is consistent with the results of Krishnan et al.
They suggested that the inherent phoria itself influences the initiation of vergence responses. In our study, phoria was grossly evaluated in all adults by covering one eye and observing the movement made by the covered eye on removal of the cover. We could not confirm the observation of Tagaki et al. The adult group mean latency was significantly longer for convergence than divergence. Thus, measurement in a large sample of subjects confirms a consistent difference in latency between convergence and divergence.
Our observation of shorter latency for divergence is compatible overall with the idea of differences in the visuomotor and attentional processes involved in the preparation of these two types of eye movements. In the children, although no significant difference in latency was found between convergence and divergence, at the individual level, in most of the children, divergence showed shorter latency than convergence.
Thus, the difference in latency, although subject dependent, was evident from childhood. The neurophysiological mechanisms involved in the initiation of vergence are not identical for convergence and divergence. For instance, Mays 32 identified at the brain stem level fewer neurons used in divergence than in convergence. It is not known whether at the cortical level, convergence and divergence activate different subcircuits, as is known to be the case in reflexive versus volitional saccades see Pierrot-Deseilligny et al.
Yarbus 34 suggested that vergence starts first, followed by the saccade and then by the residual vergence. He also suggested that during the saccade the vergence simply adds to the saccade. Subsequent studies 12 13 18 19 35 dealing with saccade—vergence interactions have questioned the second observation of Yarbus.
The initial direction and landing position of saccades
Vergence has been reported to be accelerated by the saccade and, reciprocally, saccade was decelerated by the vergence. Collewijn et al. Combined divergent movements, nevertheless, when studied with high resolution also showed presaccade divergence. The most novel result of our study is the difference between children and adults in this aspect of behavior. Children clearly show frequent asynchronous behavior, namely the preceding of the vergence component.
Moreover, our data show that the ability for synchronization develops very slowly with age and continues beyond the age of 10 to 12 years see Fig. Thus, the study of combined eye movements provides a useful tool for examining this delicate aspect of visuomotor control in children, which is presumably related to cognitive development and ability to handle multiple motor commands together. For adults, latencies of both components of combined movements were found to be longer by 20 to 40 ms than those of corresponding pure movements. This is in agreement with the study of three subjects by Takagi et al.
Once a decision to generate eye movement toward the visual target is made, activity is initiated in two independent trigger circuits: one for the saccade system and the other for the vergence system. The investigators also proposed an eventual difference in the thresholds or in the delays for triggering these two brain stem circuits. This model is thus still related to the brain stem, although it also deals with cortical aspects, such as fixation requirements. Increased latency of combined eye movements is an observation also compatible with the more general framework in the psychology—physiology literature showing that reaction time, for example, for simultaneous bimanual responses, is longer than that of unimanual ones.
Note that the difference is also small—on the order of 10 to 20 ms see Steenbergen et al. Thus, consistent with other modalities, combination of two oculomotor commands takes approximately 20 ms more. Our study shows that a similar phenomenon exists in children.
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At least one of the components of combined movements was significantly longer than that of the corresponding movement programmed alone. Variability in the length of latency was significantly larger in children for all types of eye movements. Our observations are in agreement with the study by Munoz et al.
This was attributed to poor control over visual fixation. Frick et al. They suggested that developmental and individual differences in latencies are linked to the development of the neural attentional systems that control the ability to disengage or to inhibit the visual fixation. More recently, Mostofsky et al.
According to these investigators, latency variability could reflect the prefrontal dysfunction underlying the behavioral abnormalities observed in ADHD. Thus, there is an overall agreement in various fields of research in young subjects or in pathology that increased variability of latency reflects immaturity on the control of the visual fixation system, perhaps linked to prefrontal development. Our observations in the variability of latency in the present study are compatible with this line of thinking.
Submitted for publication January 23, ; revised April 29, ; accepted May 30, Commercial relationships policy: N. The publication costs of this article were defrayed in part by page charge payment. F igure 1. View Original Download Slide. Different types of eye movements elicited with the use of the 3-D visual display. Horizontal saccades at far or at close, pure convergence, or divergence along the median plane, and combined convergent or divergent movements.
F igure 2. Typical recordings of the three types of eye movements studied. Recordings from child IS, 10 years old. The target LED appeared at time 0. Arrows : onset of each movement; dotted lines : location of the target. For combined movements, the lateral eccentricity and the depth or vergence component of the target are indicated. Note that the pure saccade is accompanied by a transient disconjugacy of convergence and divergence A. A small saccade component occurs during the pure convergence B. The vergence component of the combined convergent movement starts before the saccade C.
The vergence component of the combined divergent movement starts after the saccade D. F igure 3. Individual mean latency of saccades and vergence in children A and adults B. Means for saccades include leftward and rightward saccades at far or at close. Vergence includes pure convergence and divergence along the median plane. Vertical bars : SE. Group means are based on 15 subjects. F igure 4. Individual means of latency in saccades for far and close viewing distance in children A and adults B. Other notations are as in Figure 3.
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F igure 5. Individual mean latency with the SE for pure convergence and divergence along the median plane in children A and adults B. F igure 6. Individual mean latency with the SE for saccade and vergence components of combined movements and for correspondingly pure movements. Results from children. A , B Comparisons for combined convergent movements; C , D comparisons for combined divergent movements. F igure 7. Individual mean latency with the SE for saccade and vergence components of combined movements and for correspondingly pure saccade and vergence eye movements.
Results shown are from the adults. A , B Comparisons for combined convergent movements; C , D comparisons for combined divergent movements; other notations are as in Figure 6. T able 1. View Table. Far to Sacc.
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Close Conv. Comb Conv. Comb Div. Sacc Comp. Close Div Comp. F igure 8. Individual percentages of combined movements for which vergence starts first, vergence and saccade components start together, or saccade component starts first. Results shown are from the children A and the adults B. Vertical bars : SE of group mean.
F igure 9. A Latency of pure movements saccade and vergence as a function of age in children. B Latency of components of combined eye movements in children as a function of age. C Percentage of different types of initiation of combined movements in children as a function of their age. In all graphs, adult data are shown on the right. The authors thank Giulia A.
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Brain Dev. Age-related performance of human subjects on saccadic eye movement tasks. Exp Brain Res. Saccadic eye movements in normal children from 8 to 15 years of age: a developmental study of visuospatial attention. J Autism Dev Dis. Vergence eye Movements: Basic and Clinical Aspects. Butterworth Boston. An analysis of latencies and prediction in the fusional vergence system. Semmlow JL, Wetzel P. Dynamic contributions of the components of binocular vergence. J Opt Soc Am A. Convergence and divergence exhibit different response characteristics to symmetric stimuli.
Vision Res. Ocular vergence under natural conditions. II: gaze shifts between real targets differing in distance and direction. Voluntary binocular gaze-shifts in the plane of regard: dynamics of version and vergence. Trajectories of the human binocular fixation point during conjugate and non-conjugate gaze-shifts. Shared target selection for combined version-vergence eye movements. J Neurophysiol. Hung GK. Saccade-vergence trajectories under free- and instrument-space environments. Curr Eye Res.
Gap-overlap effects on latencies of saccades, vergence and combined vergence-saccades in humans. An accurate and linear infrared oculomotor. The Neurobiology of the Prefrontal Cortex. Richard E. Mirrors in the Brain: How our minds share actions and emotions. Giacomo Rizzolatti. Christopher Eccleston. New Frontiers in Mirror Neurons Research. Pier Francesco Ferrari. Fundamentals of Computational Neuroscience. Thomas Trappenberg. Information Systems and Neuroscience. Bruno G. Space, Time and Number in the Brain. Stanislas Dehaene. Jan vom Brocke.
Cerebral Cortex. Edmund T. Gaetano Valenza. Computational Theories and their Implementation in the Brain. Lucia M. The Neurobiological Basis of Memory. Pamela A. William R. Michael S. Neuroimaging and Psychosocial Addiction Treatment. Sarah W. Feldstein Ewing. Performance Psychology. Markus Raab. The Social Neuroscience of Intergroup Relations:. Sylvia Terbeck. The Oxford Handbook of Eye Movements.
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