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Pay Attention! Researchers Uncover Mechanism That May Clarify Meaning of Attention

Neuroscientists from Tübingen and Okasaki show that tiny eye movements filter “important” stimuli and relay them to the brain.

Neuroscientists from Tübingen and Okasaki (Japan) have uncovered a mechanism that might clarify the meaning of “attention”. This often non-quantifiable term is supposed to describe how strongly we react to a visual stimulus. An international team of neuroscientists from the Tübingen Werner Reichardt Centre for Integrative Neuroscience (CIN) and the Okasaki National Institute for Physiological Sciences (NIPS) now explain the mechanism of “attention”, not by looking at the visual system, but into the rhythm and direction of tiny eye movements that we constantly make. Their hypotheses and experimental validations are published in two back-to-back articles recently published in Frontiers in System Neuroscience. Results from four decades of research are now cast in a very different light.

Good science is supposed to be “frugal”, i.e., it ought to make use of as few assumptions and abstractions as possible. In neuroscience, the abstract concept of “attention” is a concept that is considerably less frugal than would be desirable. It is basically a black box and does not necessarily explain which processes in the brain it actually addresses – a central question of perception research today.

For several decades, “attention” was thought to be a barely definable state of certain brain regions. In visual perception, for instance, eye movements towards a stimulus are triggered in the Superior Colliculus, a part of the midbrain. The direction of attention in the brain does not react equally to all stimuli, though: when there is a high level of “attention in the sensory system, reactions are swift and intense; neuroscientists call this state “attentional capture”. A state of slow and comparatively weak reactions, on the other hand, is called “inhibition of return” (IOR). Attentional capture and IOR both follow an alternating pattern, which rides on a rhythm with approximately 10 oscillations per second.

But what causes this rhythm, and how does “attention” control it? The international research team have now been able to depict the processes which might be responsible in a surprisingly simple model. These CIN and NIPS neuroscientists have been cooperating for several years now, headed by Dr. Ziad Hafed (Tübingen). They are investigating a phenomenon whose importance for visual perception has long been underestimated: tiny eye movements, so-called microsaccades. These small adjustments constantly correct the axis of vision when the gaze fixates an object. In earlier studies, Hafed and colleagues had found that microsaccades are generated in the Superior Colliculus in a stable rhythm that is reset by new stimuli entering the visual field. Microsaccades also change direction with each iteration.

Image of a woman's eyes.

The brain filters “important” stimuli simply based on saccadic corrections of the direction of gaze. Image is for illustrative purposes only.

Following up on these observations, Hafed and his team arrived at a hypothesis: what if the rhythm and direction of microsaccades directly trigger attentional capture and IOR? They developed a theoretical and computer model based on this assumption, employing a wide range of parameters to see what predictions the model could make. Testing the model’s predictions in experiments, the researchers surprised even themselves: they found that besides microsaccades, no additional factors were necessary in the model to explain attentional capture and IOR.

Ziad Hafed states that “attention” may be explained quite “parsimoniously”. He believes that the brain filters “important” stimuli simply based on saccadic corrections of the direction of gaze. These eye movements directly produce the phenomena which have so far been described as attentional capture and IOR. Which of these two occurs depends on the timing and direction of the stimulus relative to the microsaccadic rhythm and direction. ‘These findings are a strong argument that the mechanism of “attention” is based on a very simple principle’, says Hafed. ‘Should they be validated by further studies, results from decades of research would have to be seen in a very different light.’

About this neuroscience research

Source: Universitaet Tübingen
Image Source: The image is in the public domain.
Original Research: Full open access paper for “Vision, Perception, and Attention through the Lens of Microsaccades: Mechanisms and Implications” by Ziad M. Hafed, Chih-Yang Chen, and Xiaogang Tia in Frontiers in Systems Neuroscience. Published online December 2 2015 doi:10.3389/fnsys.2015.00167

Full open access paper for “A Microsaccadic Account of Attentional Capture and Inhibition of Return in Posner Cueing” by Xiaoguang Tian, Masatoshi Yoshida, and Ziad M. Hafed in Frontiers in Systems Neuroscience. Published online March 7 2016 doi:10.3389/fnsys.2016.00023


Abstract

Vision, Perception, and Attention through the Lens of Microsaccades: Mechanisms and Implications

Microsaccades are small saccades. Neurophysiologically, microsaccades are generated using similar brainstem mechanisms as larger saccades. This suggests that peri-saccadic changes in vision that accompany large saccades might also be expected to accompany microsaccades. In this review, we highlight recent evidence demonstrating this. Microsaccades are not only associated with suppressed visual sensitivity and perception, as in the phenomenon of saccadic suppression, but they are also associated with distorted spatial representations, as in the phenomenon of saccadic compression, and pre-movement response gain enhancement, as in the phenomenon of pre-saccadic attention. Surprisingly, the impacts of peri-microsaccadic changes in vision are far reaching, both in time relative to movement onset as well as spatial extent relative to movement size. Periods of ~100 ms before and ~100 ms after microsaccades exhibit significant changes in neuronal activity and behavior, and this happens at eccentricities much larger than the eccentricities targeted by the microsaccades themselves. Because microsaccades occur during experiments enforcing fixation, these effects create a need to consider the impacts of microsaccades when interpreting a variety of experiments on vision, perception, and cognition using awake, behaving subjects. The clearest example of this idea to date has been on the links between microsaccades and covert visual attention. Recent results have demonstrated that peri-microsaccadic changes in vision play a significant role in both neuronal and behavioral signatures of covert visual attention, so much so that in at least some attentional cueing paradigms, there is very tight synchrony between microsaccades and the emergence of attentional effects. Just like large saccades, microsaccades are genuine motor outputs, and their impacts can be substantial even during perceptual and cognitive experiments not concerned with overt motor generation per se.

“Vision, Perception, and Attention through the Lens of Microsaccades: Mechanisms and Implications” by Ziad M. Hafed, Chih-Yang Chen, and Xiaogang Tia in Frontiers in Systems Neuroscience. Published online December 2 2015 doi:10.3389/fnsys.2015.00167


Abstract

A Microsaccadic Account of Attentional Capture and Inhibition of Return in Posner Cueing

Microsaccades exhibit systematic oscillations in direction after spatial cueing, and these oscillations correlate with facilitatory and inhibitory changes in behavioral performance in the same tasks. However, independent of cueing, facilitatory and inhibitory changes in visual sensitivity also arise pre-microsaccadically. Given such pre-microsaccadic modulation, an imperative question to ask becomes: how much of task performance in spatial cueing may be attributable to these peri-movement changes in visual sensitivity? To investigate this question, we adopted a theoretical approach. We developed a minimalist model in which: (1) microsaccades are repetitively generated using a rise-to-threshold mechanism, and (2) pre-microsaccadic target onset is associated with direction-dependent modulation of visual sensitivity, as found experimentally. We asked whether such a model alone is sufficient to account for performance dynamics in spatial cueing. Our model not only explained fine-scale microsaccade frequency and direction modulations after spatial cueing, but it also generated classic facilitatory (i.e., attentional capture) and inhibitory [i.e., inhibition of return (IOR)] effects of the cue on behavioral performance. According to the model, cues reflexively reset the oculomotor system, which unmasks oscillatory processes underlying microsaccade generation; once these oscillatory processes are unmasked, “attentional capture” and “IOR” become direct outcomes of pre-microsaccadic enhancement or suppression, respectively. Interestingly, our model predicted that facilitatory and inhibitory effects on behavior should appear as a function of target onset relative to microsaccades even without prior cues. We experimentally validated this prediction for both saccadic and manual responses. We also established a potential causal mechanism for the microsaccadic oscillatory processes hypothesized by our model. We used retinal-image stabilization to experimentally control instantaneous foveal motor error during the presentation of peripheral cues, and we found that post-cue microsaccadic oscillations were severely disrupted. This suggests that microsaccades in spatial cueing tasks reflect active oculomotor correction of foveal motor error, rather than presumed oscillatory covert attentional processes. Taken together, our results demonstrate that peri-microsaccadic changes in vision can go a long way in accounting for some classic behavioral phenomena.

“A Microsaccadic Account of Attentional Capture and Inhibition of Return in Posner Cueing” by Xiaoguang Tian, Masatoshi Yoshida, and Ziad M. Hafed in Frontiers in Systems Neuroscience. Published online March 7 2016 doi:10.3389/fnsys.2016.00023

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