Coupling of saccade plans to endogenous attention during urgent choices

Reviewer #1 (Public Review):

Summary:

The classical pro/antisaccade task has become a valuable diagnostic tool in neurology and psychiatry (Antoniades et al., 2013, Vision Res). Although it is well-established that antisaccades require substantially longer latencies than prosaccades, the exact attentional mechanisms underlying these differences are not yet fully elucidated. This study investigates the separate influences of exogenous and endogenous attention on saccade generation. These two mechanisms are often confounded in classical pro/antisaccade tasks. In the current study, the authors build on their previous work using an urgent choice task (Salinas et al., 2019, eLife) to time-resolve the influences of exogenous and endogenous factors on saccade execution. The key contribution of the current study is to show that, when controlling for exogenous capture, antisaccades continue to require longer processing times. This longer processing time may be explained by a coupling between endogenous attention and saccade motor plans.

Strengths:

In the classical pro/antisaccade task the direction of exogenous capture (caused by the presentation of the cue) is typically congruent with the direction of prosaccades and incongruent with antisaccades. A key strength of the current study is the introduction of different experimental conditions that control for the effects of exogenous capture on saccade generation. In particular, Experiments 3 and 4 provide strong evidence for two independent (exogenous and endogenous) mechanisms that guide saccadic choices, acting at different times. Differences in timing for pro and antisaccades during the endogenous phase were consistent and independent of whether the exogenous capture biased early saccades toward the correct prosaccade direction or toward the correct antisaccade directions.

As in previous studies by the same group (Salinas et al., 2019, eLife; Goldstein et al., 2023, eLife), the detailed analysis of the time course of goal-directed saccades allowed the authors to determine the exact, additional time of 30 ms that is necessary to generate a correct antisaccade versus prosaccade.

Overall, the manuscript is very well written, and the data are presented clearly.

Weaknesses:

The main research question could be defined more clearly. In the abstract and at some points throughout the manuscript, the authors indicate that the main purpose of the study was to assess whether the allocation of endogenous attention requires saccade planning [e.g., ll.3-5 or ll.247-248]. While the data show a coupling between endogenous attention and saccades, they do not point to a specific direction of this coupling (i.e., whether endogenous attention is necessary to successfully execute a saccade plan or whether a saccade plan necessarily accompanies endogenous attention).

Some of the analyses were performed only on subgroups of the participants. The reporting of these subgroup analyses is transparent and data from all participants are reported in the supplementary figures. Still, these subgroup analyses may make the data appear more consistent, compared to when data is considered across all participants. For instance, the exogenous capture in Experiments 1 and 2 appears much weaker in Figure 2 (subgroup) than Figure S3 (all participants). Moreover, because different subgroups were used for different analyses, it is often difficult to follow and evaluate the results. For instance, the tachometric curves in Figure 2 (see also Figure 3 and 4) show no motor bias towards the cue (i.e., performance was at ~50% for rPTs <75 ms). I assume that the subsequent analyses of the motor bias were based on a very different subgroup. In fact, based on Figure S2, it seems that the motor bias was predominantly seen in the unreliable participants. Therefore, I often found the figures that were based on data across all participants (Figures 7 and S3) more informative to evaluate the overall pattern of results.

Reviewer #2 (Public Review):

Goldstein et al. provide a thorough characterization of the interaction of attention and eye movement planning. These processes have been thought to be intertwined since at least the development of the Premotor Theory of Attention in 1987, and their relationship has been a continual source of debate and research for decades. Here, Goldstein et al. capitalize on their novel urgent saccade task to dissociate the effects of endogenous and exogenous attention on saccades towards and away from the cue. They find that attention and eye movements are, to some extent, linked to one another but that this link is transient and depends on the nature of the task. A primary strength of the work is that the researchers are able to carefully measure the timecourse of the interaction between attention and eye movements in various well-controlled experimental conditions. As a result, the behavioral interplay of two forms of attention (endogenous and exogenous) is illustrated at the level of tens of milliseconds as they interact with the planning and execution of saccades towards and away from the cued location. Overall, the results allow the authors to make meaningful claims about the time course of visual behavior, attention, and the potential neural mechanisms at a timescale relevant to everyday human behavior.

Reviewer #3 (Public Review):

Summary and overall evaluation:

Human vision is inherently limited so that only a small part of a visual scene can be perceived at a given moment. To address this limitation, the visual system has evolved a number of strategies and mechanisms that work in concert. First, humans move their eyes using saccadic eye movements. This allows us to place the high-resolution region in the center of the eye's retina (the fovea centralis) on objects of interest so that these are sampled with high acuity. Second, salient, conspicuous stimuli that appear abruptly and/or differ strongly from the other stimuli in the scene, seem to automatically attract ("exogenous") attention, so that a large share of the neuronal "resources" for visual processing is devoted to the stimuli, which improves the perception of the stimuli. Third, stimuli that are important for the current task and the current behavioral goals can be prioritized by attention mechanisms ("endogenous" attention), which also secures their allocated share of processing resources and helps them be perceived. It is well-established that eye movements are closely linked to the mechanisms of attention (for a review, see Carrasco, 2011, cited in the manuscript). However, it is still unclear what role voluntary, endogenous attention plays in the control of saccadic eye movements.

The present study used an experimental procedure involving time-pressure for responding, in order to uncover how the control of saccades by exogenous and endogenous attention unfolds over time. The findings of the study indicate that saccade planning was indeed influenced by the locus of endogenous attention, but that this influence was short-lasting and could be overcome quickly. Taken together, the present findings reveal new dynamics between endogenous attention and eye movement control, and lead the way for studying them using experiments under time pressure.

The results provided by the present study advance our understanding of vision, eye movements, and their control by brain mechanisms for attention. In addition, they demonstrate how tasks involving time pressure can be used to study the dynamics of cognitive processes. Therefore, the present study seems highly important not only for vision science, but also for psychology, (cognitive) neuroscience, and related research fields more generally.

Strengths:

The experiments of the study are performed with great care and rigor and the data is analyzed thoroughly and comprehensively. Overall, the results support the authors' conclusions, so I have only minor comments (see below). Taken together, the findings seem important for a wide community of researchers in vision science, psychology, and neuroscience.

Weaknesses (minor points):

(1) In this experimental paradigm, participants must decide where to saccade based on the color of the cue in the visual periphery (they should have made a prosaccade toward a green cue and an antisaccade away from a magenta cue). Thus, irrespective of whether the cue signaled that a prosaccade or an antisaccade was to be made, the identity of the cue was always essential for the task (as the authors explain on p. 5, lines 129-138). Also, the location where the cue appeared was blocked, and thus known to the participants in advance, so that endogenous attention could be directed to the cue at the beginning of a trial (e.g., p. 5, lines 129-132). These aspects of the experimental paradigm differ from the classic prosaccade/antisaccade paradigm (e.g. Antoniades et al., 2013, Vision Research). In the classic paradigm, the identity of the cues does not have to be distinguished to solve the task, since there is only one stimulus that should be looked at (prosaccade) or away from (antisaccade), and whether a prosaccade or antisaccade was required is constant across a block of trials. Thus, in contrast to the present paradigm, in the classic paradigm, the participants do not know where the cue is about to appear, but they know whether to perform a prosaccade or an antisaccade based on the location of the cue.

The present paradigm keeps the location of the cue constant in a block of trials by intention, because this ensures that endogenous attention is allocated to its location and is not overpowered by the exogenous capture of attention that would happen when a single stimulus appeared abruptly in the visual field. Thus, the reason for keeping the location of the cue constant seems convincing. However, I wondered what consequences the constant location would have for the task representations that persist across the task and govern how attention is allocated. In the classic paradigm, there is always a single stimulus that captures attention exogenously (as it appears abruptly). In a prosaccade block, participants can prioritize the visual transient caused by the stimulus, and follow it with a saccade to its coordinates. In an antisaccade block, following the transient with a saccade would always be wrong, so that participants could try to suppress the attention capture by the transient, and base their saccade on the coordinates of the opposite location. Thus, in prosaccade and antisaccade blocks, the task representations controlling how visual transients are processed to perform the task differ. In the present task, prosaccades and antisaccades cannot be distinguished by the visual transients. Thus, such a situation could favor endogenous attention and increase its influence on saccade planning, even though saccade planning under more naturalistic conditions would be dominated by visual transients. I suggest discussing how this (and vice versa the emphasis on visual transients in the classic paradigm) could affect the generality of the presented findings (e.g., how does this relate to the interpretation that saccade plans are obligatorily coupled to endogenous attention? See, Results, p. 10, lines 306-308, see also Deubel & Schneider, 1996, Vision Research).

(2) Discussion (p. 16, lines 472-475): The authors suppose that "It is as if the exogenous response was automatically followed by a motor bias in the opposite direction. Perhaps the oculomotor circuitry is such that an exogenous signal can rapidly trigger a saccade, but if it does not, then the corresponding motor plan is rapidly suppressed regardless of anything else.". I think this interesting point should be discussed in more detail. Could it also be that instead of suppression, other currently active motor plans were enhanced? Would this involve attention? Some attention models assume that attention works by distributing available (neuronal) processing resources (e.g., Desimone & Duncan, 1995, Annual Review of Neuroscience; Bundesen, 1990, Psychological Review; Bundesen et al., 2005, Psychological Review) so that the information receiving the largest share of resources results in perception and is used for action, but this happens without the active suppression of information.

(3) Methods, p. 19, lines 593-596: It is reported that saccades were scored based on their direction. I think more information should be provided to understand which eye movements entered the analysis. Was there a criterion for saccade amplitude? I think it would be very helpful to provide data on the distributions of saccade amplitudes or on their accuracy (e.g. average distance from target) or reliability (e.g. standard deviation of landing points). Also, it is reported that some data was excluded from the analysis, and I suggest reporting how much of the data was excluded. Was the exclusion of the data related to whether participants were "reliable" or "unreliable" performers?

(4) Results, p. 9, lines 262-266: Some data analyses are performed on a subset of participants that met certain performance criteria. The reasons for this data selection seem convincing (e.g. to ensure empirical curves were not flat, line 264). Nevertheless, I suggest to explain and justify this step in more detail. In addition, if not all participants achieved an acceptable performance and data quality, this could also speak to the experimental task and its difficulty. Thus, I suggest discussing the potential implications of this, in particular, how this could affect the studied mechanisms, and whether it could limit the presented findings to a special group within the studied population.