Measurement of Neurophysiological Signals of Ignoring and Attending Processes in Attention Control

Summary

Attention control comprises enhancement of target signals and attenuation of distractor signals. We describe an approach to measure separately but concurrently, the neurophysiology of attending and ignoring in sustained intermodal attention, utilizing a passive control condition during which neither process is continuously engaged.

Abstract

Attention control is the ability to selectively attend to some sensory signals while ignoring others. This ability is thought to involve two processes: enhancement of sensory signals that are to be attended and the attenuation of sensory signals that are to be ignored. The overall strength of attentional modulation is often measured by comparing the amplitude of a sensory neural response to an external input when attended versus when ignored. This method is robust for detecting attentional modulation, but precludes the ability to assess the separate dynamics of attending and ignoring processes. Here, we describe methodology to measure independently the neurophysiological signals of attending and ignoring using the intermodal attention task (IMAT). This task, when combined with electroencephalography, isolates neurophysiological sensory responses in auditory and visual modalities, when either attending or ignoring, with respect to a passive control. As a result, independent dynamics of attending and of a ignoring can be assessed in either modality. Our results using this task indicate that the timing and cortical sources of attending and ignoring effects differ, as do their contributions to the attention modulation effect, pointing to unique neural trajectories and demonstrating sample utility of measuring them separately.

Introduction

Attention control guides behavior by directing our neural and cognitive resources toward select input signals, while restricting access to other signals, based on a given behavioral goal ¹. For instance, when reading a book, the visual signals corresponding to the book are the target signals to be enhanced, whereas other sensory signals — such as the TV in the next room — are distractor signals to be attenuated. Recordings in both human and non-human primates ^1-4, indicate that neural responses in sensory cortices are enhanced for attended targets relative to ignored distractors during selective attention, indicating that the strength of sensory inputs in the brain is modulated as a function of whether they are classified as targets or distractors ^5-7. We refer to this difference in signal strength when attending versus ignoring as the attention modulation effect.

Of increasing interest is the question of whether and how the neural processes of attending contribute to attention control and its impairments, separately from the neural processes of ignoring. It is increasingly clear that the ability to ignore distractions can be impaired independently from our ability to attend targets. For instance, distractor-suppression can be impaired with increased task load ⁸, cognitive aging ⁹ and sleep deprivation ¹⁰, without a decrement in target enhancement. It is not currently known if a decrement in target enhancement can also exist without a deficit in distractor suppression. Perhaps more importantly, it is not resolved whether deficits of either attending or ignoring, but not both, can elucidate neuropsychiatric conditions in which attention control is impaired. As such, it is valuable to better understand whether attending and ignoring arise from separable cortical pathways, if and how they differ in neural dynamics. By measuring attending and ignoring processes separately, such questions can be addressed.

Here we describe methodology to measure the neurophysiological signals of attending and ignoring separately, but concurrently, in sustained attention. This approach builds on the attention modulation effect: the difference in amplitude of a neural sensory response when the individual is attending versus ignoring to stimuli in that sensory stream. The attention modulation effect is a powerful tool for detecting attention modulation over sensory signals, but it precludes the ability to assess the separate dynamics of attending and ignoring processes. Namely, a difference in neural sensory responses when attending versus ignoring could arise because the process of attention enhances sensory target signals, or because ignoring attenuates sensory distractor signals, or both. To test between these alternatives, the use of an additional control condition is required in which one quantifies the strength of sensory inputs at their natural baseline, when they are neither attended nor ignored. This is similar to walking down a busy street full of cars, but neither actively watching (e.g., for a taxi) nor actively ignoring (e.g., non-taxi cars and buses) the passing cars. By evaluating sensory signals that are attended or ignored, relative to a passive reference condition, the magnitude and timing of attending and ignoring processes can be quantified separately.

Effective uses of such a passive control in measuring attending and ignoring processes have been reported previously in studies of anticipatory attention ^11-13 and memory-attention interactions ^9,10,14-17. Here we describe the use of this approach in the context of sustained attention, in a non-cued, continuous, intermodal (i.e., auditory-visual) attention task (IMAT) ¹⁸. In other words, this method is appropriate to the study of ongoing rather than preparatory control processes, allowing for tracking of these processes across time. This method also quantifies control processes that modulate sensory responses across different sensory modalities (i.e., auditory versus visual), thus focusing on processes that are not specialized to within a particular sensory or content domain. Unlike previous functional magnetic resonance imaging studies ^15,19,20, this method tracks attending and ignoring processes using temporally resolved neurophysiological signals (electroencephalography, EEG), thus providing millisecond resolution on the temporal profiles of attending and ignoring processes. Our representative results demonstrate the use of the technique in identifying direct evidence for separable cortical sources and temporal dynamics of the neural processes of attending and ignoring, and unique contributions to the attention modulation effect.

Protocol

NOTE: This study protocol was developed in accordance with the ethical guidelines approved by the investigational review board at University of California Los Angles.

1. Preparation of Auditory and Visual Stimuli

1. Using software in which visual images can be generated, create two gray scale sinusoid gratings, approximately 5.7 inches in diameter and of any frequency (e.g., 1.36 cycles/degree of visual angle). The images will have an on-screen duration of 100 msec.
   1. Tilt one of the gratings about 10 visual degrees to the right off the median, and tilt the other grating the same amount to the left of the grating.
   2. Ensure that the degree of the tilt is sufficient to allow the participants to distinguish a left tilt from a right tilt without relying on guessing.
2. Using software in which auditory tones can be generated, create two pure tones of 100 msec duration.
   1. Make one of the tones of a higher pitch and the other of a lower pitch. For instance, one pitch can be 750 Hz and the other 900 Hz.
   2. As for the visual stimuli, ensure that the tones are sufficiently distinct such that participants can distinguish between them without relying on guessing.

2. Programming of Stimulus Presentation

1. Using presentation software, create the computer code that will control the presentation of the auditory and visual stimuli during the experiment.
   1. First select the number of stimuli to be presented. Present at least 150 of each of visual and auditory stimuli per experimental condition, to ensure that there are enough repetitions for a reliable neurophysiological response.
   2. Present visual stimuli centrally on a gray background, with the participant sitting at a comfortable viewing distance. Present the auditory stimuli through speakers positioned on either side of the screen.
      Note: For visual stimuli we recommend a gray background, with RGB values at the mid-point (128,128,128) between pure white (255,255,255) and pure black (0,0,0), with the white and black used in generation of the sinusoid stimuli. This ensures that the mean brightness of the background and stimulus are comparable, and the contrast is constant between any point in the stimulus and the background.
   3. For each of auditory and visual stimuli, independently select the timing for the stimuli.
      Note: This prevents participants from anticipating stimuli based on temporal relationships between the two streams.
   4. Use an inter-stimulus interval (ISIs) of approximately 1 sec between sequential presentations of stimuli from the same modality. Slower ISIs will make the task more demanding on vigilance, faster ISIs may make it impossible for participants to make their responses in time.
   5. Vary the precise ISI randomly within a range, such as 0.7 to 2 sec, to make the stimuli unpredictable to participants, preventing neural responses associated with anticipation.
   6. Because cross-modal interactions can arise from simultaneously or near-simultaneously presented stimuli ^21,22, keep the ISI between stimuli from two different streams at no less than 300 msec.
2. Ensure that the auditory and visual stimuli appear to occur interleaved to the participants, but never co-occurring.
3. Last, divide the stimuli into segments of twenty-five. These segments will be preceded by one of the three randomly selected task instructions, described in the next section.

3. Task Instruction

1. Orient the participant to the task prior to collecting neurophysiological measures of brain activity.
   1. Instruct participants to attend and respond to the auditory tones and to ignore the visual stimuli when the instruction is “Listen”. Present this instruction both through audio and visual means.
   2. Assign two buttons for participants to make responses to each tone. For example, “press the left arrow if the tone is high, and right arrow if the tone is low” when the instruction is “Listen”.
   3. Similarly, instruct participants to attend and respond to the visual gratings and to ignore the auditory stimuli when the instruction is “Look”.
   4. Assign two buttons for participants to make responses to the visual gratings. For example, “press the left arrow if the grating is tilted to the left, and right arrow if the grating is tilted to the left”.
      1. Use the same two buttons for visual stimuli as for auditory stimuli to enhance the interference between the modalities and therefore the need to employ attention control mechanisms.
   5. Finally, instruct participants to make no responses when the instruction is “Passive”, but ensure that participants keep their eyes open and focused on the screen.
2. Throughout the task session, alternate the instructions for “Listen” and “Look” between segments to switch a previously attended modality to being irrelevant, thus making it a potent distractor.
3. Remind the participants to keep their eyes fixated on the middle of the screen, or a small dot or crosshair presented at the location of the visual stimulus, and to keep their eyes open throughout the experiment.
4. Build in eight to ten second breaks between segments to mitigate effects of fatigue, allow the participants to rest their eyes, as well as longer 1-2 min breaks every 6-8 min.
5. Finally, provide each participant with ample practice to ensure that they are performing the task correctly. It may be beneficial, especially for participants who have attention difficulties, to practice the visual and the auditory tasks with the attended stream presented in isolation, without the concurrent presentation of the distractor stream.

4. Neurophysiological Data Collection

1. Once the participants are familiar with the task, begin collection of neurophysiological responses to attended and ignored signals during the IMAT.
2. Prepare the electroencephalography (EEG) cap and recording equipment according to manufacturer instructions, and in accordance with current methodology and publication standards for EEG research ^26,27.
   Note: Important EEG recording parameters for EEG recording during the IMAT, that can be user specified, include: (a) sampling rate of 128-1,024 Hz, to capture the low-frequency of ERP signals; (b) alternating current (AC) recording to minimize slow drift; (c) net with sampling of entire scalp and with at minimum of 64 sensors, if source imaging analyses are to be performed.
3. Apply the cap to the participant’s scalp and verify signal impedance and quality at each of the sensors. Pay special attention to ensure that impedances of the recording electrodes are uniform and within the range recommended by manufacturer.
   Note: At this time, also add any additional physiological measurement devices if wanting to collect non-neural physiological signals such as respiration or pulse.
4. Synchronize the neurophysiological recordings with the stimulus presentation software and neurophysiological recording software according to manufacturer’s instructions.
5. Record the neurophysiological signals while the participant performs the task, ensuring that the recording software has precise record of the timing of each stimulus and response for subsequent analysis.

5. Offline Data Analysis

1. Prepare the neurophysiological data for statistical analysis using analysis software.
2. First, remove non-neural signal components that will contribute variability to the neurophysiological recordings of brain responses.
   1. Use a high-pass filter of 0.1-1 Hz, to remove slow drifts such as those caused by changes in impedance of the sensors.
   2. Use a low-pass filter of 30-50 Hz to remove high frequency components introduced by electrical noise.
   3. Identify sensors that show unreliable data, and exclude these or interpolate the signals.
   4. Identify and eliminate large infrequent noise components such as muscle artefact from jaw contraction or movements of the forehead, and systematic, non-neural contributions, such as eye movements.
      Note: Typical algorithms to remove non-neural components include independent components analysis and regression, as well as iterative algorithms based on explicit selection criteria (e.g., voltage changes that exceed a threshold). Follow guidelines of available analysis software, and proceed in accordance with current standards for EEG research ^26,27.
3. Once major non-neural components of the neurophysiological data have been removed, re-reference the data at each electrode by subtracting from each sensor the mean across all other sensors or the mean across left and right mastoid channels.
   Note: This step re-expresses the effects at each sensor relative to a neutral reference that is assumed to contain zero neural signals.
   Note: Sparser electrode montages may not have sufficient sampling to meet the assumptions of this technique ^26,27. In the latter case, the mean of the left and right mastoid may provide a more accurate reference.
4. Next extract temporal epochs of approximately 1 sec surrounding each auditory and each visual event shown. Include 100 msec preceding the stimulus onset to serve as a baseline interval and at least 600 msec following the stimulus onset.
5. Average the data from all epochs that fall into the same condition — attended, ignored, and passively perceived stimuli — to compute the average evoked response potential or “ERP”. Subtract the mean of the data in the pre-stimulus baseline to re-express the ERP amplitudes as changes relative to the pre-stimulus signal.
6. To identify the time course of attending processes, compare the amplitude and timing, as well as spatial distribution of the ERP response after attended stimuli, against those during the passive condition.
7. To identify the time course of ignoring, compare the amplitude and timing, as well as spatial distribution of the ERP response after ignored stimuli, against those during the passive condition.

Results

The IMAT protocol has been used previously to identify the unique contributions of attending and ignoring processes to response speed during sustained attention ¹⁸. In that study, we tested 35 healthy right-handed individuals (22 female, age: x̅ = 21.0, σ = 5.4), recruited through the Psychology department subject pool at the University of California, Los Angeles. All participants provided written informed consent prior to participating in the study. Representative results highlight the value of measuring atte...

Discussion

Processes related to attending and to ignoring in attention control may involve different neural pathways and time courses. Therefore, it is of value to measure these processes separately. The IMAT is a tool, by which one may capture neurophysiological signals of attending and ignoring separately, but concurrently, in sustained attention. The critical steps include the measurement of sensory neurophysiological responses when the participant is attending, ignoring or passively perceiving stimuli presented in a given modal...

Materials

List of materials used in this article

Name	Company	Catalog Number	Comments
NetStation Software	Electrical Geodesic, Inc.	version 4.5.1	Alternate recording software may be used.
Matlab Software	The MathWorks, Inc.	7.10.0 (R2010a)	Alternate analysis and presentation software may be used.
PsychToolbox Software	http://psychtoolbox.org/	v3.0.8 (2010-03-06)	Open-source software. Alternate stimulus presentation software may be used.
Netstation Amplifier	Electrical Geodesic, Inc.	300	Alternate amplifier may be used.
EEG Net	Electrical Geodesic, Inc.	HCGSN130	Alternate EEG cap may be used.
Saline-Based Electrolyte (Potassium Chloride)	Electrical Geodesic, Inc.	n/a	Electrolyte used in soaking of net for this high-impedance EEG system. Alternate electrolyte mediate can be used.