Elsevier

Neuroscience Letters

Volume 554, 25 October 2013, Pages 6-10
Neuroscience Letters

Refining the time course of facilitation and inhibition in attention and action

https://doi.org/10.1016/j.neulet.2013.08.055Get rights and content

Highlights

  • Action-centred attention holds that action and attention systems are coupled.

  • Motor output is an expression of attentional mechanisms.

  • Present work tested timecourse of excitation and inhibition in attention and action.

  • Manifestation of inhibition in action lagged 200–300 ms behind attention.

  • Attentional mechanisms cascade to coupled motor system.

Abstract

According to action-centred models of attention, there is a tight coupling between attention and response planning processes. In support of these models, previous research has shown that reach trajectories deviate towards a cue at short (<100 ms) cue-target onset asynchronies (CTOAs) and away from a cue presented at longer CTOAs (>750 ms). These deviations resemble the pattern of facilitatory and inhibitory reaction time (RT) effects observed in keypress studies. Here, participants reached to targets following a non-predictive cue and 5 CTOAs (from 100 to 600 ms in 125 ms intervals) were used to gain a deeper understanding of the relationship between RT and trajectory effects. Consistent with action-centred attention, facilitatory and inhibitory cuing after-effects were present in RTs and trajectories. Interestingly, RT and trajectory effects were temporally staggered: facilitatory effects were present in trajectories at the 100 ms CTOA when they had already dissipated in RTs, and inhibitory effects were present in RTs (≥350 ms CTOAs) before they were detected in trajectories (600 ms CTOA). The time courses of the cuing effects suggest that, although action and attention systems are tightly coupled, the facilitatory and inhibitory mechanisms operate in attention before affecting action planning.

Introduction

According to action-centred models of attention [5], [15], [19], the processes of attention and movement planning are intricately linked. Two main predictions are derived from this tenet. First, the processes of action planning influence the distribution and capture of attention. The findings that different stimulus features capture attention in different action contexts and that perceptual processes are enhanced at a movement endpoint support the prediction that action systems shape attention [2], [7], [23]. Second, the dedication of attention to an object automatically generates a response that will allow the individual to interact with that object. Studies showing that movement characteristics are affected by non-target information support this second prediction [11], [18], [20]. The latter influence of attention on action is the focus of the present work.

The cue-target task has been used to examine the time course of facilitatory and inhibitory processes following the capture of attention [14]. Participants respond to a target that is presented at one of several potential target locations. The key manipulation is that the target appears at various time intervals (cue-target onset asynchronies or CTOAs) after a non-predictive cue is presented at one location. Keypress studies that use this method report shorter reaction times (RTs) to targets at cued locations than at uncued locations at short (<150 ms) CTOAs, but longer RTs to cued targets than uncued targets at longer CTOAs (>300 ms [12], [14]). The early facilitatory effect is thought to occur because attention was drawn to the location of the cue, which increases the efficiency of information processing at that location relative to uncued locations. Because the cue does not predict the target location, however, attention is subsequently withdrawn from the cued location. The withdrawal of attention is thought to have two consequences. First, the facilitatory cuing effect is short-lived (peaking at approximately 100 ms CTOA). Second, an inhibitory coding is activated for the cued location. The inhibitory coding is thought to hinder the return of attention to and/or information processing at the cued location leading to longer RTs for cued than for uncued targets at longer CTOAs.

To investigate the influence of attentional mechanisms on more complex actions [1], [17], several researchers have asked participants to execute rapid goal-directed aiming movements in cue-target contexts [3], [10], [13]. The focus of these studies was comparing movement trajectories to cued and uncued target locations [11], [17], [20]. Relative movement trajectories have proved to be a sensitive index of attention/action coupling because the direction of reaching movements are represented, in part, by a specialized set of directionally-tuned cells within cortical motor systems [8]. Multiple directionally-tuned cells fire for a given movement and the initial direction of the executed movement is derived from the vector sum of the firing rates of a collection of directionally-tuned cells. Importantly, multiple subpopulations of directionally-tuned cells that represent separate responses may be active simultaneously [6]. The predicted behavioural consequence of this multiple-response representation is that the direction/curvature of the subsequent movement will be determined by the summation of the co-existing responses – excitation of a non-target response leads to trajectory deviations towards the non-target stimulus, whereas inhibition of a non-target response to below baseline levels leads to deviations away from the non-target stimulus [21], [22].

Recently, Neyedli and Welsh [13] analyzed the characteristics of movements executed in a cue-target task with CTOAs of 100, 350, 850, and 1100 ms. It was predicted that if attention and action are intricately linked, then movement trajectories should reflect the attentional mechanisms operating at movement onset – trajectories should deviate towards the cued location at short CTOAs when attention excites the cued response, but away from cues at long CTOAs when the cued response has been inhibited. Although the predicted patterns of effects were generally present, there was evidence for a temporal offset in the manifestation of the mechanisms. At the 100 ms CTOA, there were significant deviations towards the cue, but there were no significant cuing effect in RTs. For the longer CTOAs (≥350 ms), RTs for cued targets were longer than for uncued targets suggesting the presence of inhibitory mechanisms in attention. Reliable trajectory deviations away from the cued location, however, were not observed until the 850 ms CTOA suggesting that the inhibitory mechanism acting on the motor system took longer to affect behaviour. Thus, it was suggested that, although attention and action are tightly coupled, the mechanisms of facilitation and inhibition may operate in attention-dominated systems before cascading to motor centres. Although these data provided initial insight into coupled attention/action mechanisms, the relatively large CTOAs did not provide sufficiently refined evidence for the cascading explanation and for time course of coupled attention/action mechanisms.

The present study was designed to gain a finer understanding of the timing of the facilitation and inhibition mechanisms in attention and action by examining the spatiotemporal characteristics of aiming movement executed in a cue-target task with a narrower range of CTOAs. The CTOAs of 100, 225, 350, 475, or 600 ms were chosen for three reasons. First, they are consistent with the CTOAs over which one expects to observe facilitatory and inhibitory cuing effects. Second, there was a standard interval of 125 ms to provide a finer and more consistent resolution of the time course than in previous work. Finally, the 100 and 350 ms intervals were used in the previous study [13] to enable a replication of available data.

Section snippets

Participants

Eighteen (11 female) right-handed members of the University of Toronto community volunteered to participate. Participants were 18–28 years old, had normal or corrected-to-normal vision, and were naïve to the purpose of the study. The procedures conformed to the Helsinki Declaration and were approved by Office of Research Ethics at the University of Toronto. Informed consent was obtained prior to data collection and participants received 10 CAD.

Apparatus, stimuli, task and procedure

Participants stood at a table in front of a 38 × 30 cm

Temporal measures

Because only movements to the centre location were analyzed, cued target trials were those on which both the cue and target were presented at the centre location. Uncued target trials were those on which the central target was preceded by a cue in the left or right location. RTs and MTs on movements following left and right cues were averaged together to derive a single value for uncued target condition. Mean RTs and MTs were submitted to a 2 (Target Location: cued, uncued) × 5 (CTOA: 100, 225,

Discussion

The present study was conducted to assess the temporal relationship between the facilitatory and inhibitory mechanisms of attention and action planning by analyzing the spatiotemporal characteristics of aiming movements to targets presented after non-predictive cues. The pattern of effects observed here was consistent with the predicted tight coupling between attention and action: movements deviated towards the cued location at short CTOAs and away from the cued location at longer CTOAs.

Conclusions

In the present study, a detailed assessment of the time course of excitatory and inhibitory mechanisms resulting from non-predictive cues was conducted. The data suggest a delay in the manifestation of excitatory and inhibitory mechanisms in measures of response initiation and programming because the expression of the excitatory and inhibitory influences was observed in RT before they were observed in movement trajectories. These data are consistent with and significantly extend previous

Acknowledgements

This research was supported by a Canada Foundation for Innovation grant (LT), an Early Research Award from the Ontario Ministry of Research and Innovation (TNW), and Discovery Grants (TNW, LT) and a post-graduate scholarship (HN) from the Natural Sciences and Engineering Research Council of Canada. We thank Drs. Matthew Heath, Paul van Donkelaar, Howard Zelaznik, Carlos Gómez, and anonymous reviewers for their comments on an earlier version of the paper.

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