Category: News and Blog

A commentary on “Visual attention is not limited to the oculomotor range” by Hanning, Szinte & Deubel (2019)

We read with great interest the recent PNAS paper by Hanning and colleagues, in which they use a variant of Craighero et al’s Eye Abduction paradigm to test the proposal that exogenous covert attention is constrained by the oculomotor range (Smith & Schenk 2012; Casteau & Smith 2019). If you’re not familiar with the paradigm, figure A illustrates the setup. The idea is that by abducting the eye by ~35-40 degrees it is possible to present stimuli at locations that can be seen but cannot be reached with a saccadic eye-movement. This neat procedure decouples perception and oculomotor control, and in 2012 we showed that peripheral cues beyond the oculomotor range did not summon attention (Smith, Rorden & Schenk 2012).

In the Hanning version of the task participants are shown 4 channels of noise, 3 within the range of eye-movements and one beyond. One of the locations is cued for 50ms, and 100ms later a probe appears in one of the channels for 50ms. Participants must report the orientation of the probe with button press. People are really bad at this task, and accuracy is only above chance at the cued location. Critically, this attentional facilitation for the cued location is observed even when the cued channel is beyond the range of eye-movements, contrary to our previous findings. Hanning and colleagues argue this is problematic for premotor theory, and argue the data are more consistent with selection-for-action models like VAM. They conclude that covert, exogenous orienting of attention is not constrained by the range of eye-movements, contrary to our previous findings.

The paper is beautifully presented, the experiment is cleverly designed and on first inspection these data look clear cut. There can be no doubt that the peripheral cues are producing enhanced target detection. So, do we need to abandon our position that covert, exogenous orienting is dependent on oculomotor activation? Perhaps not yet. Hannings’ data are convincing, but as they note in their paper, there are considerable differences in the stimuli used in our lab (e.g. Smith et al., 2012, Casteau & Smith 2018), by Craighero et al., (2012) and by Michalczyk et al., (2018) that show an effect of eye-abduction on covert attention, and those used by Hanning and colleagues. One potentially crucial difference is the difficulty of the task. Hannings’ task is extremely difficult. In fact, it is impossible to accurately discriminate the target unless it is attended (See fig 2b: dprime is ~0 at all uncued locations – you can see the task for yourself here). To understand why this is a problem we need to first consider the rationale for using a non-predictive peripheral cueing task. The reason typically given is that a non-predictive cue gives the participant no incentive to endogenously attend to the cued location, so allows a ‘pure’ measure of exogenous attention. This rationale makes sense when the task is simple detection task or a speeded discrimination, because the participant detects the target regardless of whether or not it appears at the cued location, and the differences emerge in the speed of target detection. However, this rationale does not hold true when the task is so difficult that the target is never detected at uncued locations. Why? Because under these conditions the cue is highly informative from the perspective of the participant; they only ever perceive a target when they attend a cued location, and never detect targets at uncued locations (a similar issue is found in the change blindness literature- see Smith & Schenk 2010). It therefore makes complete sense for participants to adopt an attentional set of ‘endogenously attend cued location’ in order to correctly perform the task. We know that endogenous shifts of attention can be observed at short SOAs, for example in Muller & Rabbit (1989) seminal study there is a beneficial effect of endogenous attention at 100ms SOA, and Tipples (2002) has shown a similar effect for arrows. It therefore seems likely that the peripheral cue used by Hanning et al., engaged both endogenous and exogenous attention, and it was the endogenous component of attention that produced the attentional benefit. If participants are endogenously attending the cued location, the results are in fact in exact accordance with our previous findings and those of Klein and colleagues (1980;1994), which were that endogenous orienting is independent of oculomotor control. A less critical, but still noteworthy issue is that the sample is rather small (n=6 in the critical covert attention task). In contrast, papers showing impaired exogenous attention beyond the oculomotor range tend to have larger samples (N= ~20-25), so there is also a risk that this study was somewhat underpowered to detect the interaction of interest. Hanning et al., also make the valid point that previous studies using eye-abduction did not establish the range of eye-movements for their participants. However, in our 2018 paper we measured each participants own oculomotor range, and again showed a selective deficit for covert exogenous attention at locations beyond the range of eye-movements when the eye was centred in its orbit .

To briefly summarize, Hanning et al., show that a peripheral cue produces attentional facilitation beyond the EOMR. The evidence for this effect is very clear, and we do not dispute that participants did indeed covertly orient to the cued location. However, we do dispute the claim that this shift of attention is exogenous in nature. Rather, we believe it is more likely that participants endogenously oriented to the peripheral cue because it was the only way to successful complete the task, and that the improved performance at the cued location is caused by this endogenous shift of attention. We agree with the conclusion that the data are problematic for premotor theory, but only because they show that endogenous orienting is possible to locations that cannot become the goal of a saccade.

We asked Hanning & colleagues if they would like to reply to our comment, and will add it here ASAP if they do. Nina will be joining us in Durham for our workshop and we’re looking forward to some lively discussions! (there are still some places if you fancy joining us)

 

References

  • Casteau, S.; Smith, D.T. Covert attention beyond the range of eye-movements: Evidence for a dissociation between exogenous and endogenous orienting. Cortex [Google Scholar] [CrossRef]
  • Casteau, S & Smith, D.T. (2019). Associations and Dissociations between Oculomotor Readiness and Covert Attention. Vision 3: 17.
  • Craighero, L.; Nascimben, M.; Fadiga, L. Eye position affects orienting of visuospatial attention. Biol.2004, 14, 331–333. [Google Scholar] [CrossRef]
  • Hanning, N., Szinte, M,. & Deubel H. Visual attention is not limited to the oculomotor range. Proceedings of the National Academy of Sciences 2019, 116 (19) 9665-9670; DOI: 10.1073/pnas.1813465116
  • Klein, R.M. Does oculomotor readiness mediate cognitive control of visual attention? Perform. 1980, 8, 259–276. [Google Scholar]
  • Klein, R.M.; Pontefract, A. Does Oculomotor Readiness Mediate Cognitive Control of Visual Attention? Revisited! In Attention and performance XV: Conscious and Nonconscious Information Processing; Umiltà, C., Moscovitch, M., Eds.; The MIT Press: Cambrige, MA, USA, 1994; pp. 333–350. [Google Scholar]
  • Smith, D.T.; Schenk, T. The Premotor theory of attention: Time to move on? Neuropsychologia 2012, 50, 1104–1114. [Google Scholar] [CrossRef]
  • Michalczyk, L.; Paszulewicz, J.; Bielas, J.; Wolski, P. Is saccade preparation required for inhibition of return (IOR)? Lett. 2018, 665, 13–17. [Google Scholar] [CrossRef] [PubMed]
  • Smith DT & Schenk, T. (2010). Inhibition of return exaggerates change blindness. Quarterly Journal Of Experimental Psychology 63(11): 2231-2238.
  • Smith, D.T. Smith, D.T.; Schenk, T.; Rorden, C. Saccade preparation is required for exogenous attention but not endogenous attention or IOR. Exp. Psychol Hum. Percept. Perform. 2012, 38, 1438–1447. [Google Scholar] [CrossRef] [PubMed]

 

Daniel T. Smith & Soazig Casteau,

Dept of Psychology, Durham University UK

Tasty review paper published in Vision

Last summer Soazig and I were approached about writing a review article on oculomotor readiness hypothesis / premotor theory for a special issue of Vision on “Eye Movements and Visual Cognition”. This was a very tempting opportunity, and I must admit I was flattered to be courted by psychology bigwigs like Klein and Liversedge, but I had a couple of reservations. Firstly, this is quite a crowded field, and there had already been some excellent reviews of the literature, including one I had written with Thomas Schenk just a few years ago. Did we really have something new to say? Could we produce something that offered more insight than just describing recent developments in the field? Secondly, writing any paper is time consuming, but with the pressures of the imminent REF there is a distinct disincentive to publishing papers that are not eligible for submission, such as review papers. On the flip side, writing a review seemed like a a great opportunity to articulate the theoretical ideas about attention and eye-movements that we had been bubbling around over the last few years and in the end the decision was easy.

We spent quite some time kicking round ideas for a structure and two key concepts formed the basis of the review. Firstly, that it was absolutely critical to explicitly a differentiate between presaccadic attention, covert endogenous attention and covert exogenous attention. Secondly, that the evidence from neuropsychological studies had been rather neglected in favour of psychophysical or neurophysiological evidence. Once we had these ideas, the review started to fall into place and we were able to develop our key lines of argument, which were (1) presaccadic attention is qualitatively different from covert attention, so studies of presaccadic attention don’t speak to oculomotor readiness / premotor theory per se (2) The neuropsychological evidence for a mandatory coupling between covert exogenous orienting and saccade programming is pretty strong, but the evidence is actually really weak for a causal link between endogenous attention and saccade programming. In the end we felt convinced that the evidence was most convincing for an oculomotor readiness theory of exogenous orienting, (hence the snazzy acronym of OREO) and we hope you will read the paper and be convinced too!

The paper is open access, and you can find it here: https://www.mdpi.com/2411-5150/3/2/17/htm

Casteau, S & Smith, D.T. (2019). Associations and Dissociations between Oculomotor Readiness and Covert Attention. Vision 3: 17.

Writing this review has been an interesting process, as it touches on some conceptual issues that Soazig and I have been struggling with over the last few years. One thing I have never understood is why saccade deviation away from an attended location is often cited as evidence for premotor theory. Everyone says it, but it makes no sense! Surely the saccade should be deviated towards the attended location if it’s associated with a saccade programme? Maybe now someone will explain it to me at our upcoming workshop on attention and motor control (all welcome 😊): http://motorbiasproject.com/workshop

My internship at Durham University: A blogpost by Bianca Biebl from Ludwig Maximilians Universitat

When I embarked on my journey to travel from Munich to Durham for six weeks, I kept wishing that I was already there. That I already knew my accommodation was okay, my colleagues at university friendly and my tasks neither mind-numbing nor overcharging. Upon arrival I soon realized that my accommodation was really nice – even though a bit far from city centre. And regarding my internship, not only did I immediately feel like part of a team with my two supervisors but I also had a great task, which I knew would benefit me greatly for my academic growth. Of course, designing, programming, recruiting, testing and analyzing EyeTracking data was not an easy task. However, with every error message that I managed to resolve by myself and with every additional student I successfully tested, my self-confidence grew and in the end I could actually present a well-working experiment and proper results. This feeling of accomplishment was further encouraged by the supportive feedback by my supervisors and the mutual brainstorming for new ideas to improve every little detail. I also really appreciated the open-mindedness of everyone at university regarding any question I had, which made me feel really welcome. Another aspect of my internship I thoroughly enjoyed was a weekly event, where researchers and PhD students listened to various talks by external scientists while having a glass of wine. Some of my most memorable moments however were surely made during the weekends, where I explored the beautiful surrounding areas like the seaside, Newcastle, York or Edinburgh. The only thing I felt was missing from my time in Durham was contact with other people inside and outside of work. Since I was mostly working on my own, had the office to myself for great periods of time and spent evening and weekends alone, I would have liked to e.g. have more regular meetings or eat lunch together. Altogether however, I had a wonderful time in this beautiful city, learned a great deal and met some truly lovely people.  

Some advice for anyone thinking about a research internship at Durham University 

  • AirBnbs are a great way to stay at Durham – look for ones close to university and city centre 
  • Find a supervisor who is interested in the same topics as you are – there is really something for everyone here 
  • Take care of your network access beforehand  – it takes a few weeks 
  • People at university (colleagues / reception) or in the tourist office in town will help you with any problems – just ask 
  • Use Durham’s amazing location to travel around the north of England – it’s worth it! 

MotorBias Workshop speaker update: Dr Monika Harvey

We’re delighted to announce that Dr Monika Harvey  from University of Glasgow will give a talk at our MotorBias workshop in Durham this July. Monika has a particular interest in disorders of attention such as hemispatial neglect, and has done fascinating research on how the motor system can be used to help patients with neglect. Click HERE to find out a lot more about Monika’s research!

Thoughts on Prof Tim Hodgson’s seminar on Development of Oculomotor Control

I was  delighted to welcome Prof Tim Hodgson from Lincoln University to Durham to give a seminar on his recent work exploring the development of oculomotor control in young children. His talk drew on a series of experiments conducted at the Lincoln Summer Scientist event where Tim and his team examined oculomotor behaviours in children as young as 3! The surprising result (to me at least!) was that very young children seemed to experience a ‘sticky fixation’, such that their gaze remained locked at fixation when a target jumped from fixation to the periphery, or when gaze cues were used to direct saccades. Gaze cues automatically activate saccade programmes in adults (e.g. Kuhn & Kingstone 2009), so the fact that these young children don’t reflexively follow gaze cues suggested to me that perhaps gaze-cueing is a learned, rather than instinctual behaviour (Cole Smith & Atkinson 2015). More provocatively, Tim also argued that even though the children’s eyes were ‘stuck’ at fixation, they were nevertheless able to covertly orient into the periphery. I harrumphed my approval at this little bit of premotor theory bashing but was mindful it was based on the observation that children were able to accurately report the appearance of a peripheral target, even though they failed to execute a saccade towards it. As Bob Kentridge suggested, perhaps there was overactive fixation which prevents the release of a saccade but not the programming of the saccade. All in all it was a fascinating and thought-provoking seminar. We then retired to the Vic for refreshments and further discussion.

Kuhn, G., & Kingstone, A. (2009). Look away! Eyes and arrows engage oculomotor responses automatically. Attention Perception & Psychophysics, 71(2), 314-327. doi:10.3758/app.71.2.314

Cole, G.G., Smith, D.T. & Atkinson, M.A. (2015). Mental state attribution and the gaze cueing effect. Attention, Perception, & Psychophysics 77(4): 1105-1115.

Dan Smith