Introduction

Our behaviour is adapted flexibly to meet our task goals. Selective attention research has revealed that predictions about the locations or other features of relevant events can bias neural activity starting from early stages of perceptual analysis [1], [2], [3], [4], [5], [6]. It has become increasingly evident that predictions about the timing of events also play a major role in organising and optimising behaviour [7], [8]. However, compared to spatial attention, relatively little is known about the functional mechanisms by which temporal expectations alter performance.

Like spatial orienting of attention, temporal orienting has been proposed to occur in an endogenous or exogenous fashion [9]. In spatial attention, exogenous orienting is an involuntary focusing of attention driven by an inherently salient or transient cue (also referred to as stimulus driven, automatic, bottom-up). Endogenous orienting, on the other hand, is understood as a voluntary, intentional focus of attention to a specific location, usually guided by a symbolic cue (also referred to a goal directed, controlled, top-down) [10], [11].

In spatial attention studies, the properties of exogenous and endogenous orienting are well established. Behavioural results have demonstrated that the effect of endogenous spatial orienting varies with task demands (i.e. increases with probability of cue validity), while effects of exogenous cues are independent of cue validity [12]. Studies have also suggested that exogenous cues are less susceptible to interference [12], and harder to ignore than endogenous cues [10]. Another common finding is that exogenous cues induce faster and more transient effects than endogenous orienting [13], [14].

In a recent review, Coull and Nobre [9] have suggested a distinction between endogenous and exogenous attention in the temporal domain. Exogenous temporal orienting is proposed to be generated automatically by exposure to stimuli with rhythmic or predictable temporal structure [9], [15], [16]. On the other hand, endogenous temporal orienting is proposed to be engaged in tasks that use informative, symbolic cues to direct attention in time [17], [18], [19]. Behaviourally, the effect of temporal orienting of attention has been observed both in studies using symbolic [17], [20], [21], [22], [23] as well as rhythmic cues [15], [24], [25], [26]. However, the extent to which these two different types of cues rely upon two dissociable attentional mechanisms remains unknown.

In this experiment, we adapted the task from Doherty and colleagues [15] to test for separable effects of temporal orienting based on predictions from the intrinsic rhythmic structure of events and based on instructive symbolic cues. In our task, a ball moves across the screen of a computer monitor in discrete steps and passes ‘under’ an occluding band (see Figure 1). The participants' task is to make a speeded discrimination of a shape contained within the ball when it reappears from under the occluder. We used a factorial design to manipulate temporal expectations formed on the basis of the rhythmic temporal structure of dynamic events versus explicit symbolic cues. The temporal structure of the events was either rhythmic or arrhythmic. In rhythmic (valid) trials, the duration of each ball stimulus and of the time-step in between successive balls was constant. These parameters provided precise temporal predictions for the duration of the occlusion period, and were always valid. In arrhythmic (neutral) trials, intervals between successive balls varied randomly, providing no prediction for the duration of the occlusion period. The presence or absence of the isochronous rhythm was crossed factorially with the presence or absence of symbolic cues to predict the duration of the occlusion period. The colour of the ball acted as a symbolic cue. In trials with valid symbolic cues, the ball colour predicted the duration of the occlusion interval with 100% validity; in neutral trials the colour provided no information about the duration of the occlusion period. There were no invalid cueing conditions in the task. The design, therefore, resulted in the symmetrical and orthogonal crossing of type of temporal prediction (valid or neutral) carried by each cue type (rhythmic or symbolic).

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Figure 1. Schematic of the task.

A coloured ball appears at the left side of a grey screen and moves across the screen in seven steps. After reaching the occluding band, the ball disappears behind for a single step. When the ball reappears it contains either an upright (50%) or a tilted (50%) cross. Temporal expectations could be induced by the rhythm and/or the colour of the balls preceding the occlusion.

https://doi.org/10.1371/journal.pone.0014620.g001

In order to test whether expectations built from the temporal structure of events versus from symbolic cues were under cognitive control, we also manipulated task instructions in a factorial fashion. Participants were told to use the information provided by rhythm (“attend to speed”) or the colour of the balls (“attend to colour”) in different blocks. If, as we predict, temporal expectations induced by the temporal rhythm of the events are ‘exogenous’, they should not be contingent upon or affected by participants focusing on this source of information. On the other hand, if, as we predict, temporal expectations induced by symbolic cues are ‘endogenous’, they should come under cognitive control and be significantly influenced by instruction to use this source of information. Having established two separable forms of temporal orienting, we were also interested in testing whether these two sources of bias show strong interactions or whether they operate mainly independently, resulting in additive effects.

Materials and Methods

Results

To analyse the behavioural consequences of expectations driven by rhythmic versus symbolic temporal cues under different task instructions, RTs from correct responses were submitted to a repeated-measures analysis of variance (ANOVA), testing the three factors of instruction (speed vs. colour) rhythmic cues (valid vs. neutral) and symbolic cues (valid vs. neutral). As explained in the methods, only the data from the short-occlusion period provide a pure measure of the effects of temporal expectation.

Performance accuracy was high (average 90.4%) and did not differentiate between conditions (lines in Figure 2), revealing no main effects or interactions between rhythmic or symbolic cueing [Fs(1, 17) <4.08, ps>.05]. In line with previous temporal orienting studies, RT values provided a sensitive measure of the effects of temporal expectations [30]. The analysis revealed main effects of rhythmic [F (1, 17)  = 36.23, p<.001] as well as of symbolic cues [F(1, 17) = 8.80, p = .009] (Figure 2a). For both cue types, valid temporal predictions speeded reaction times when compared to neutral conditions. However, whilst the effect of the temporal rhythmic cues was independent of instruction (main effect of rhythm), there was an interaction between symbolic cues and instruction [F(1, 17) = 7.03, p = .017] (Figure 2b). Post hoc subsidiary analyses with Bonferroni adjustment for multiple comparisons demonstrated that the validity effect of the symbolic cues was only observed if associated with the “attend-to-colour” instruction [F(1, 17) = 10.50, p = .005]. There were no significant effects involving the interaction between temporal expectations driven by rhythms and by symbolic cues [Fs(1, 17) <.36, ps>.55].

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Figure 2. Reaction times results.

(a) Main effect of temporal rhythms and symbolic cues (b) Effects of temporal rhythms and predictive cues broken down by task instructions. The bars represent reaction time values left y-axis), and accuracy data is represented by the lines (right y-axis). Error bars represent standard errors of the means (SE).

https://doi.org/10.1371/journal.pone.0014620.g002

As expected, no differences were observed after the long occlusion period where the conditional probability of target events was equated across all trial types [Fs (1, 17) <2.23, p's>.10].

Discussion

By using a factorial design to manipulate temporal expectations based on rhythms and symbolic cues in an orthogonal and symmetrical fashion, we provide direct evidence for the existence of qualitatively separable means of orienting of attention in time, which may be analogous to exogenous and endogenous mechanisms established in spatial orienting [9].

Similar to its spatial counterpart [12], [31], [32], [33], [34], ‘exogenous’ temporal orienting is triggered by stimulus properties and proceeds automatically. Our results confirm that the isochronous temporal rhythm of events automatically facilitates performance, regardless of whether participants strategically focus on the temporal structure of the events. This exogenous orienting appears to generate temporal expectation incidentally and automatically, allowing participants to anticipate the moment of target appearance and facilitating the perceptual discrimination process. On the other hand, symbolic cues were only effective if participants focused strategically on the information provided by the cues and voluntarily oriented their attention to the time predicted by the cue. This ‘endogenous’ type of orienting was therefore was goal-directed and strictly under top-down control.

Our results further suggested that exogenous and endogenous orienting reflect two sources of top-down biases acting upon the information-processing stream. The lack of interaction between temporal predictions carried by rhythms versus symbolic cues support the interpretation of two independent and additive mechanisms of temporal attention, at least at the processing stages that determine reaction-time performance. Further experimentation testing the effects of exogenous and endogenous effects on different behavioural measures and in different task contexts will be required to verify the generalisability of the current findings (c.f., [35], [36]). It will also be of great interest to test whether more complex, non-isochronous predictable rhythms are similarly able to induce exogenous temporal orient to facilitate performance, or whether, as the rhythms become more complex, it becomes necessary to engage voluntary, top-down mechanisms in order to benefit from learned temporal predictions [37], [38].

Our findings support Coull and Nobre's [9] proposal for a dissociation between automatic (exogenous) and goal-directed (endogenous) temporal orienting. We have also introduced a novel paradigm that allows the study of exogenous and endogenous temporal attention independently, on a trial-by-trial basis, and without requiring extensive training. Future studies are necessary to investigate the neural substrates underlying these two different orienting mechanisms of temporal attention.

Acknowledgments

We would like to thank Angel Correa and Mariagrazia Capizzi for their contribution in the development of this task.