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Competition between bottom-up and top-down mechanisms of auditory attention: neurophysiological and physiopathological mechanisms of distractibility

Final Report Summary - DISTRACTIBILITY (Competition between bottom-up and top-down mechanisms of auditory attention: neurophysiological and physiopathological mechanisms of distractibility.)

Attention is the brain function by which we, voluntarily or not, improve the processing of specific information while other stimuli are disregarded. The entry of information to the brain is controlled by top-down and bottom-up processes. Voluntary or top-down attention enables the good performance of an on-going task by selecting the relevant information. One’s attention can also be involuntarily captured by an unexpected salient stimulus and thus diverted from the previously on-going task. This bottom-up form of attention is necessary to be aware of potentially important (but irrelevant to the on-going task) event (e.g. fire alarm), and is commonly referred as distractibility. A good balance between bottom-up and top-down mechanisms is thus crucial to be task-efficient while being aware of our surrounding environment.
Lack of distractibility points to the dominance of top-down attention, whereas enhanced distractibility could be due to either reduced efficiency of top-down mechanisms, or enhanced triggering of bottom-up attentional capture. This precarious balance is often affected in neurological or psychiatric disorders, such as attention-deficit hyperactivity disorder, bipolar disorder, stroke... Despite the obvious importance of distractibility in assessing the patients’ neurological status, no index of this process has been validated in clinical practice. Currently available tests of attention are suitable for revealing impairment in top-down attention, but they fail to indicate any alteration in bottom-up attentional capture.
Therefore, this project aims at proposing a new paradigm to assess both bottom-up and top-down attention mechanisms, and at understanding how these mechanisms dynamically interact in the healthy or pathological human brain.
In a first study, using non-invasive scalp EEG in 15 healthy subjects, we found that increasing top-down attention reduces early processing of distracting sounds, but fail to protect from bottom-up attentional capture and to reduce the behavioral distraction cost. Moreover, the impact of bottom-up attentional capture by distracting sounds could disturb top-down mechanisms by lengthening target processing and detection.
This first study was pursued in 38 healthy subjects to compare the EEG attentional markers according to their dream recall frequency. High dream recallers present larger EEG markers of top-down attention and an enhanced processing of distracting sounds. These results suggest that high dream recallers benefit from enhanced capacities in both top-down and bottom-up attention.
To localize the different brain markers of attention, this project was complemented by recording magnetoencephalography signal in 15 healthy subjects. Analysis is in progress.
In a second study, intracortical EEG was recorded from electrodes located in the auditory cortices of 16 patients with intractable epilepsy, implanted with electrodes for surgical purposes. The first results suggest that sustained and oscillatory brain responses are modulated by top-down attention within the auditory cortices. Further analysis will be performed to explore the processing of distracting sounds and how bottom-up and top-down attentional mechanisms dynamically interact within the auditory cortices.
In a third study, scalp EEG data were recorded in 9 patients with damage of the lateral prefrontal cortex to specify the role of this brain region in top-down and bottom-up mechanisms of attention. Damage of the lateral prefrontal cortex was found to result in reduced top-down attention, enhanced distracting sound processing and delayed reorientation of attention, speaking for an imbalance in attention towards increased distraction.
A behavioral study was performed in patients suffering from bipolar disorders (n=11) or schizophrenia (n=19) to specify their attentional capacities. Both patients with schizophrenia or bipolar disorders presented a preserved balance between top-down and bottom-up attention. However, only patients with bipolar disorders suffered from a reduction in cognitive resources that impact their performances in context of high task load.
This project proposes a new paradigm which provides a good way to behaviorally and neurophysiologically estimate the distraction effect of isolated unexpected sounds outside the attentional focus, with no or little contamination from change in arousal. Using this new test, this project provided crucial information into the brain functioning of the balance between bottom-up and top-down attentional mechanisms in the healthy brain. Moreover in patients with stroke in the frontal cortex, it was shown that the lateral prefrontal cortex is involved in the control of both top-down and bottom-up attention, and play a crucial role in the attentional balance and in the level of distractibility.
It was also possible to measure the attentional balance in different populations and specify how this precarious equilibrium can be knock of balance and lead to attention impairments. As stated previously, there is no test of distractibility that is currently used in clinical practice. Therefore this new paradigm constitute a powerful tool to measure bottom-up and top-down mechanisms of attention and to provide an index of distractibility, that could be used for clinical purposes.