An analysis of the dependence of saccadic latency on target position and target characteristics in human subjects

Specialization of the foveal region of the human retina necessitates a sophisticated ocular motor system to translate an image appearing on the peripheral retina onto the fovea: this is achieved by the generation of saccadic eye movements which effect rapid fixation of the target. The saccadic latency which is the time from the presentation of the target to the commencement of the saccade consists of the transmission times in the afferent and efferent pathways and the central processing time which is likely to be appreciable due to the complexity of the pathway. An important centre in the generation of saccades is the superior colliculus [1]. While a direct projection from the retina via the superior brachium leads to activation of the visual cells of the superior colliculus, the dominant pathway is via the primary visual cortex [2] which projects to the superior colliculus through the thick cytochrome oxidase stripes of area V2 [3]. Saccadic movements are also driven consciously from the frontal eye fields (area 8) which have a projection to the superior colliculus [4]. For a saccade to be generated, there must be activation of the saccade-related burst neurones of the deep layers of the superior colliculus: these drive the excitatory burst neurones of the paramedian pontine reticular formation (PPRF), which in turn drive the extra-ocular motor neurones. There must also be disengagement of the fixation neurones of the foveal representation (rostral zone) of the superior colliculus: these would otherwise drive the omnipause neurones of the PPRF, which in turn inhibit the excitatory burst neurones [5, 6]. Saccade generation thus requires release from the inhibitory actions of the fixation neurones; consequently removal of the fixation point prior to presentation of the target causes a marked shortening of the saccadic latency. This has become known as the gap effect and leads to the generation of express saccades of latency of 90–120 ms [7, 8]. When the fixation point remains visible (the overlap condition), regular saccades of latencies of 200–220 ms are generated though faster regular saccades of latencies of 135–170 ms have additionally been reported [9].

At first sight it might seem that more peripheral targets might generate saccades with a longer latency due to the more extended conduction pathway across the retina. However, in primate, peripheral ganglion cells possess faster axonal conduction velocities than their centrally located counterparts, so much so that excitation will arrive at the lateral geniculate nucleus 7 ms earlier for stimulation at 40 deg than at 10 deg (calculated from [10]). The expectation is thus that saccadic latencies should at least remain invariant with respect to the retinal location of the target and so provide a standard time reference against which the saccade is generated. However, several studies report, using a non-gap stimulus paradigm, that saccadic latencies increased with increasing target eccentricity, sometimes by considerable amounts: for example, increases as large as 60 ms have been reported [11]. Given that the conduction time in the more peripheral part of the afferent pathway is not increasing and the time delay from the peak of the saccade-related burst response in the superior colliculus to the start of the saccade is only 20 ms [1, 5, 6], such an increase in saccadic latency implies a considerable increase in central processing time. This inference, however, is at variance with respect to the major function of the peripheral retina in underlying the rapid detection of visual objects, which is mediated through the magnocellular visual pathway. Generally, those studies which reported a consistent increase in saccadic latencies [11–16] employed stationary red light emitting diodes or red neons as targets, which contrasts with those studies reporting no change which used a moving spot and a stationary white target [17, 18]. In addition to the target characteristics, the direction of gaze has been reported to have an effect in that adoption of an eccentric direction of gaze reduced the saccadic latency markedly [11, 16]. This factor has been invoked as a confounding factor to account for the reported constancy of saccadic latency [11].

Our aim was, therefore, to resolve the issue of how saccadic latency is related to target displacement. To this end, we have by employed a comprehensive range of stimulus conditions in order to determine the effects of targets which were stationary or moving, of normal intensity or of reduced red intensity, and whether the targets were viewed with the eyes directed straight ahead or at an eccentric direction of gaze. A preliminary report of part of this work has previously been published [19].

We have undertaken an investigation of the effects of target eccentricity on the latency of saccade generation with target presentation during steady fixation (overlap condition). The outcome of this study was that saccadic latency remained invariant with respect to the magnitude of target displacement, irrespective of whether the target was moving or stationary, whether fixation was straight ahead or was directed eccentrically, or whether the target was of normal intensity or consisted of a dim red target. From an examination of the outcomes of regression analysis of all the types of experiment undertaken, out of 32 experiments in 11 different subjects, P _slope did not attain statistical significance in 27 cases. In 5 cases, in which P _slope < 0.05, the relationships were discounted as unimportant [20]. We also confirmed the validity of the results for saccadic movements in both leftwards and rightwards directions and for monocular recordings. The distribution of our saccadic latencies (Fig. 1G &1H) which was similar to those reported previously [18, 21] fell predominantly into the slow regular group though the faster saccades would qualify as fast regular saccades [9]. Express saccades were never observed which is consistent with the overlap mode of target presentation. Since our data were collected in triplets, there was plainly some prior knowledge of the target location though is without effect on saccadic latencies [22].

Thus, with respect to saccadic latency, the present study confirms previous results for a normal intensity moving target [17] for a normal intensity stationary target [18] and for a yellow-green target in excess of 3 logarithmic units above foveal threshold presented in the nasal hemifield outside of the foveal area [15], but has contradicts other studies [11–14, 16]. The previous report that the saccadic latency was reduced by as much as 60 ms on adoption of an eccentric direction of gaze [11] was also not confirmed: our results indicated unequivocally that there was no such reduction in latency, which is consistent with evidence of an absence an effect of proprioceptive feedback on position sense of the eye in man [23, 24].

We have also shown constancy of saccadic latency with increasing target angular displacement, whether the target was of normal intensity or was of dim red intensity, which was all the more remarkable in that the effective intensity of the red target relative to the photopic threshold was very low. This result differs from the reported increase in saccadic latency in response to a red target of luminance up to 3 logarithmic units above foveal threshold [15]. However, the latter result is unexpected since, in the same study, a yellow-green target which was photopically equivalent to the red target resulted in essentially constant saccadic latencies [15]. The difference may have arisen on account of the very deep red target (660 nm) which was used: this may also explain the difference from the present results showing constancy of latency. When the intensity of a blue/green target was reduced by 2 logarithmic units, the saccadic latency in response to a small target displacement of 6 deg was increased by 40 ms [25], though this result reflects operation in the scotopic range since the subjects were dark adapted for 40 min prior to the experiments.

The explanation proposed to account for the large increase in saccadic latency with target angular displacement was that it allowed time for the generation of a compensatory head movement [11]; however, should the head not move, the saccadic latency would still remain greatly extended. The difference between our results and those of the previous studies are not readily reconcilable except previously reported results are not as clear cut as they may seem. Many studies had very small sample sizes. Hallet and Lightstone [13] reported an increase in saccadic latency in one subject and no change in the other while the results of Zambarbieri et al. [16] contradict those of an earlier study in which saccadic latency remained constant [26]. In the data of Fuller [11] despite, in many cases, an apparent monotonic relationship between saccadic latency and target angular displacement, none of the correlation coefficients for iso-orbital viewing were statistically significant.

Our results showing constancy of saccadic latency are, however, fully consistent with the inferences which may be drawn from primate conduction velocity data [10] in that there should be no increase in conduction time for stimulation of more peripheral parts of the retina. Furthermore, we have shown that the specific nature of the stimulus is not critical: it may be stationary, moving or of reduced intensity but the saccadic latency remains invariant. This accords with studies in primates trained to undertake fixation of novel objects appearing in the peripheral visual field: saccadic latencies were similar in response to the presentation of novel objects which differed in hue, luminance and size from the surrounding objects [27].

Our result has relevance to attempts to model the control system for saccadic eye movements. Recent models show an emphasis on explaining the gap effect. In neuronal terms, this can be viewed as the prior disenabling of the fixation neurones by extinction of the fixation point thus removing this stage in the saccade generation process [6] though more recently it has been shown express saccade generation is better predicted by the activity of buildup neurones of the superior colliculus [28]. Thus, for a gap between fixation extinction and target presentation of a fixed value (usually 200 ms), this may be regarded as a visual cue to the subject that the target is about to be presented [29, 30]: under these circumstances, it is thus not surprising that express saccades should be generated. However, in keeping with previous studies which investigated the effects of target eccentricities, we have used an overlap paradigm which requires both the disengagement of fixation and generation of the saccade.

Winner-take-all models are based on the operation of reciprocal inhibition between two competing centres such that, should one centre dominant, it becomes subject to positive feedback resulting in saccade generation [31, 32]. The values of saccadic latency generated by Clark's model are, however, unrealistically high for both the gap and overlap conditions and show a strong dependence on target intensity [31]. Saccadic latency showed a reduction with increasing target eccentricities over a limited range, though latency became asymptotic for targets in excess of 5 deg [31]. By contrast, in Findlay & Walker's model, it is proposed that the generation of an unequivocal salience peak in response to the target presentation through a non-linear triggering process leads to a "fixed and stereotyped burst of activity"[32]. The defining characteristic is the location of the burst in the salience map rather than on other characteristics like intensity. This is consistent with our results.

In the three loop model [33], the delays between the proposed three central modules are proposed to arise from stochastic variations in inputs without invoking the need for inhibitory interactions. This model does not examine the dependence of saccadic latency on target eccentricity but it does generate latency values which correspond to the present results for an overlap paradigm. However, the chosen response latency for visual cortical neurones of 30 ms is unrealistic since the conduction time from the retinal ganglion cells to the lateral geniculate nucleus is of this order of magnitude [10], irrespective of the retinal delay and conduction from lateral geniculate nucleus to visual cortex. Since the brain stem mechanisms for saccade generation have very short time delays between neurones which operate in a pulsatile manner, the overall time delay in the motor pathway amounts to only 20 ms [1, 5, 6]. Hence, the major component of delay is thus afferent and central. This is reflected in the Robinson model which incorporates a 0.2 s delay for processing of the target position in space [5]. There was no explicit provision for an increased delay as the target displacement increases. On the basis of the present results, this is indeed unnecessary. The reason for invariant saccadic latencies probably lies at the level of the retina: the sensitivity to the appearance of a peripherally located target is likely to be high since luminance detection is mediated by both M retinal ganglion cells (parasol ganglion cells) [34] and P retinal ganglion cells (midget ganglion cells) [35]. Furthermore, luminance detection would be accentuated by the steepness of the response-luminance contrast relationship of M retinal ganglion cells [36]. Thereafter, in the visual pathway, increasing target eccentricities do not lead to longer conduction times [10]. Hence, there is a strong neural basis as to why saccadic latencies should not increase with increasing target eccentricity or reduced target intensity. This is what is implied by the present results in which saccadic latency remains remarkably constant.

In conclusion, irrespective of the nature of the stimulus- a moving or stationary target, of normal or reduced intensity, viewed either directly or eccentrically- saccadic latency remains remarkably invariant with respect to target angular displacement. The corollary of this result is that there is therefore no increase in the central processing time under these conditions.