Premature saccades: A detailed physiological analysis

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Highlights

  • We studied premature saccades, which have abnormally short latencies and a curved trajectory.

  • Saccade direction and amplitude are specified almost simultaneously in 100–150 ms.

  • Saccades made before this minimum time may not necessarily be anticipatory.

Abstract

Objective

Premature saccades (PSs) are those made with latencies too short for the direction and amplitude to be specifically programmed. We sought to determine the minimum latency needed to establish accurate direction and amplitude, and observed what occurs when saccades are launched before this minimum latency.

Methods

In Experiment 1, 249 normal subjects performed the gap saccade task with horizontal targets. In Experiment 2, 28 normal subjects performed the gap saccade task with the targets placed in eight directions. In Experiment 3, 38 normal subjects, 49 patients with Parkinson’s disease (PD), and 10 patients with spinocerebellar degeneration (SCD) performed the gap saccade task with horizontal targets.

Results

In Experiment 1, it took 100 ms to accurately establish saccade amplitudes and directions. In Experiment 2, however, the latencies needed for accurate amplitude and direction establishment were both approximately 150 ms. In Experiment 3, the frequencies of PSs in patients with PD and SCD were lower than those of normal subjects.

Conclusions

The saccade amplitudes and directions are determined simultaneously, 100–150 ms after target presentation. PSs may result from prediction of the oncoming target direction or latent saccade activities in the superior colliculus.

Significance

Saccade direction and amplitude are determined simultaneously.

Introduction

Movements of the limb or even the eyes take some processing time before they are launched. For saccades, the processing time can be measured by the latency at which they are initiated after a visual target is presented. In the visually guided saccade (VGS) task, for example, subjects first foveate a fixation point at the center, and when a target appears peripherally and simultaneously with the fixation offset, the subjects are required to look quickly at the target. The latency of a VGS usually ranges from 120 to 200 ms. A histogram of latency across a large number of trials indicates that the latency falls into several peaks: early (120–135 ms), fast regular (140–180 ms), and slow regular saccades (200 ms) (Fischer et al., 1993). In addition to these, saccades with latencies shorter than the normal range rarely occur, and form a separate group of around 80–120 ms, called express saccades (Fischer et al., 1993).

Dissecting the time required for saccade generation, it would take 40–60 ms for visual information to reach the visual cortex, 20–40 ms for cortico-cortical transmission from the occipitoparietal to the frontal cortex, and finally 30–40 ms for oculomotor commands from the frontal lobe to generate eye movements (Khayat et al., 2009, Dorris and Munoz, 1998, Dorris et al., 1997, Edelman and Keller, 1996, Sparks et al., 2000, Sparks, 2002, Heeman et al., 2014, Heeman et al., 2017). All these would add up to a processing time of approximately 100 ms. Indeed, the minimal physiological visually triggered saccadic response time (minimal visual SRT) is estimated around 80–120 ms (Heeman et al., 2019).

Express saccades are made with a latency slightly above the minimal visual SRT (100–120 ms). With this short latency, there is little time left for visuospatial programming to take place from the frontal and parietal lobes, and some advance saccade programming should already be taking place when the trigger (start signal) for saccades is provided (Paré and Munoz, 1996, Leigh and Zee, 2006). Such saccades are encountered under specific conditions, e.g., when subjects are required to make saccades toward the same target position repeatedly in consecutive trials in the gap saccade [GS] task, a version of the VGS task. In this task, a gap interval is inserted between the times of fixation point offset and target presentation (Paré and Munoz, 1996, Carpenter, 2001, Munoz and Schall, 2003).

Saccades can sometimes be triggered before the processing (programming) of their metrics is hardly complete, i.e., before the amplitude, duration, and direction are fully programmed and specified. Using the gap paradigm, we found that saccades are sometimes prematurely launched with a latency even shorter than 100 ms. These saccades are often initially launched in the wrong direction (i.e., in the direction opposite of the target) with a saccade size well short of the target eccentricity, and are followed by a corrective saccade in the correct direction. Postulating that the saccades are prematurely launched when they are still incompletely programmed, we termed them prematurely initiated saccades, or premature saccades (PSs).

In this investigation, we studied the origin of PSs. Why and how do they occur? Is there a transition between PSs, express saccades, and regular saccades? Postulating that PSs with short latency represent those incompletely programmed, which of the two saccade parameters, direction or amplitude, is determined first? Would the trajectory of saccades performed with a regular latency be straighter, when there is enough time for saccade processing? Are PSs whose processing is already prepared or underway unmasked by the deficient inhibitory control of saccades? To answer these questions, we presented targets not only horizontally but also in eight different directions (i.e., horizontal, vertical, and oblique). Also, we recorded them in normal subjects and patients with neurological diseases (Parkinson’s disease [PD] and spinocerebellar degeneration [SCD]) in whom impaired inhibitory control of saccades is expected. We predicted that, due to deficient inhibitory control of saccades in these patients, PSs would be more frequently observed than in normal subjects.

Section snippets

Experimental setting

249 normal subjects (age: 39.6 ± 20.0 years; 116 male, 133 female) participated. Horizontal saccades were recorded by electrooculography (EOG) as described in our previous studies (Okano et al., 2010, Terao et al., 2016b, Terao et al., 2013a, Terao et al., 2007, Terao et al., 2016a, Terao et al., 2013b, Terao et al., 2011, Terao et al., 1998, Yugeta et al., 2010). Briefly, horizontal EOG recordings were made by two Ag-AgCl gel electrodes placed at the bilateral outer canthi, and vertical EOGs

Experiment 1. Horizontal saccades recorded by electrooculography (two-direction task)

Fig. 4A shows the traces of saccades in the GS task in a subject. Although most saccades were initiated around 200 ms after the target was turned on, some saccades were initiated earlier than 200 ms. Some saccades were off-directional saccades initially directed to the opposite side of the target, which then turned back to the target, crossing the line of origin.

The relationship between the latency and amplitude of saccades in all the subjects is plotted in Fig. 4B, with each dot representing

Discussion

Using the gap saccade paradigm, we characterized the nature of PSs as having a short latency centered around 50 ms, i.e., in the express saccade range or even shorter (Fig. 4B). The initial direction of PS was essentially unrelated to the target or saccade direction, and its amplitude was not related to target eccentricity (Fig. 4B, C, 5B–E); in the horizontal task, saccades were frequently initiated in the opposite direction of the target, followed by another saccade toward the target, with an

Conflict of interest statement

Dr. Tokushige was supported by a Research Project Grant-in-aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (19 K17046), and has received a speaker’s honoraria from Otsuka Pharmaceutical Co., Ltd.

Dr. Hamada was supported by MEXT KAKENHI (Nos. 15 K19476, 15H01658, 16H01605, and 18 K07521).

Dr. Ugawa received grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan (Nos. 25293206, 15H05881,16H05322, and

Acknowledgments

We would like to thank Dr. Hideki Fukuda for the experimental setup, data acquisition, and analysis. We also thank all of the healthy volunteers and patients for their participation.

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