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Cross-modal deactivations during modality-specific selective attention
© Mozolic et al; licensee BioMed Central Ltd. 2008
Received: 17 June 2008
Accepted: 25 September 2008
Published: 25 September 2008
Processing stimuli in one sensory modality is known to result in suppression of other sensory-specific cortices. Additionally, behavioral experiments suggest that the primary consequence of paying attention to a specific sensory modality is poorer task performance in the unattended sensory modality. This study was designed to determine how focusing attention on the auditory or visual modality impacts neural activity in cortical regions responsible for processing stimuli in the unattended modality.
Functional MRI data were collected in 15 participants who completed a cued detection paradigm. This task allowed us to assess the effects of modality-specific attention both during the presence and the absence of targets in the attended modality.
The results of this experiment demonstrate that attention to a single sensory modality can result in decreased activity in cortical regions that process information from an unattended sensory modality (cross-modal deactivations). The effects of attention are likely additive with stimulus-driven effects with the largest deactivations being observed during modality-specific selective attention, in the presence of a stimulus in that modality.
Modality-specific selective attention results in behavioral decrements in unattended sensory modalities. The imaging results presented here provide a neural signature (cross-modal deactivation) for modality-specific selective attention.
Our perception of the environment is shaped by the combination of information from multiple sensory modalities. While there are distinct regions of the cortex devoted to processing information gathered by each of the sensory systems, areas once thought to be modality-specific are now known to be influenced by input from other sensory modalities. For example, activity in both the auditory and visual cortices can be amplified by contextually or spatially congruent multisensory stimuli [1–3]. Additionally, unisensory auditory, visual, and somatosensory stimuli that are known to activate the corresponding sensory cortex can also significantly decrease activity below baseline levels in sensory cortices that process information from modalities in which no stimulus is presented [4, 5]. We use the term "cross-modal deactivations" to refer to these activity decreases that occur across sensory domains.
In addition to incoming sensory information, top-down modulation from frontal and parietal cortices can also influence activity in the sensory cortices [6–10]. Focusing attention on a particular spatial location or stimulus feature has been shown to enhance activity in regions of visual cortex responsible for processing that information, while suppressing activity in surrounding cortical areas [8, 11, 12]. Such modulations in cortical activity can even be observed in the absence of any stimuli, indicating that they can be produced solely by attentional effects independent of an actual stimulus [13–15].
These mechanisms of visual spatial attention have been studied extensively, however, less is known about the impact that attention to a single sensory modality has on sensory processing. Behavioral experiments demonstrate that the primary effect of modality-specific attention is decreased processing of stimuli in an unattended modality, while task performance in the attended modality experiences little to no improvement [16, 17].
Imaging data consistently demonstrate that focusing attention on stimuli in one sensory modality increases activity in cortical regions that process stimuli in the attended modality [18–27]. Additionally, a number of studies also show that selective attention to stimuli in one sensory modality can modulate the unattended sensory cortex by suppressing activity)[19–22, 26–28]. For example, Johnson and Zatorre (2006) demonstrated that when participants attended to shapes and ignored melodies, activity increased in visual association cortex and decreased in auditory processing regions compared to conditions where participants passively viewed these same bimodal stimuli. Although these imaging studies suggest an important role for modality-specific attention in modulating activity in both the attended and unattended sensory cortices, it is unknown to what extent modulatory effects are dependent on the presence of a stimulus. That is, decreases in auditory cortex activity during attention to visual stimuli could be produced by the stimulus itself, by top-down modulation of the sensory cortices, or by interactions between bottom-up stimulus properties and top-down attentional processes. In a study by Baier and colleagues (2006), attentional modulation of early auditory and visual cortices was found to be stronger when bimodal stimuli were expected to be associated than when the auditory and visual components of the stimulus were independent. The results of this experiment indicate that modality-specific attention can alter cortical activity prior to the presentation of a target; however the presentation of bimodal stimuli in all trials may have precluded the observation of deactivations in sensory-specific cortices.
During behavioral experiments, prominent performance decrements are observed for targets in the unattended modality. This suggests that an important neural consequence of modality-specific selective attention is the suppression of activity in sensory cortices that process stimuli in the unattended modality. Behavioral experiments that are designed to test performance enhancements and decrements associated with modality-specific attention require the presentation of stimuli in both the attended and unattended sensory modality. However, presenting bimodal stimuli may confound investigations into the physiological effects of modality-specific attention because a bimodal stimulus increases activity in both the attended and unattended sensory modality cortices, thus masking true cross-modal deactivations. To characterize the nature of the neural response to auditory and visual selective attention, this experiment utilized attention cues presented prior to unimodal sensory stimuli. On selected trials, the unimodal target was not presented after the cue, allowing us to explore increases and decreases in primary auditory and visual cortex activity due solely to attention. We hypothesized that suppression of sensory cortices during modality-specific selective attention would be evident in deactivations of the unattended sensory cortex during presentation of the cue alone.
Fifteen adult volunteers (6 men, 9 women), age 21 to 30 (mean age, 23) participated in this study. All participants were in good health, with normal or corrected to normal vision and normal hearing. After receiving an explanation of the study procedures, all participants provided written informed consent. This study was approved by and conducted in accordance with the Wake Forest University School of Medicine Institutional Review Board for the protection of human subjects.
Participants completed a cued detection paradigm that included visual and auditory targets designed to asses the effects of modality-specific attention in the presence and absence of target stimuli. In order to ensure that participants would effectively deploy attention on all trials, participants were told that all trials would contain a target following an attentional cue. They were instructed that the purpose of this experiment was to evaluate brain responses to a discrimination task of graded difficulty, so the experiment would include a range of easy to very difficult detection trials. Some auditory and visual targets provided a very small change in stimulus intensity from resting or background levels of stimulation and were very difficult to detect, while others conveyed a larger intensity change and were very salient and easy to detect. Additionally, on 1/3 of the trials, no target was presented after the cue. These "no-target" trials were included to assess the effects of attention, independent of stimulus presentation; however, participants were unaware of their existence as it was difficult to tell no-target trials apart from trials with very faint stimuli. Although including a smaller proportion of no-target trials than target trials reduces the power to detect the effects of the no-target stimulus condition, it was necessary to limit these trials so that participants remained unaware of the absence of a stimulus.
Subjects were instructed to fixate on a white cross in the center of a black screen throughout the experiment. Each trial began with a visually presented cue that provided information about the upcoming target type. A picture of two ears cued subjects to listen for an auditory target. A picture of two eyes cued subjects to look for a visual target. A picture of one eye and one ear cued subjects to pay attention to both vision and audition, as the target could appear in either modality. Additionally, there was a rest cue (two X's) that informed participants to do nothing until the next trial, and a motor cue (two fingers) that prompted subjects to press either button as soon as any target was detected. The no-target trials were different than rest trials, where participants received a rest cue, which alerted subjects that there would be a rest interval instead of a target. The rest and motor and trials were not utilized for any of the analyses included in this paper.
Following the presentation of the cue (500 ms duration), there was a variable delay (1000–1500 ms) before the target stimulus. Each auditory target was a single 50 ms, 500 Hz tone that could vary in volume from 1% to 66% of the volume of a tone adjusted for each participant to a level that could be heard clearly above the scanner noise. Six different volume gradations were created (1%, 5%, 25%, 35%, 50%, and 66% of a suprathreshold stimulus) using the volume reduction function in Goldwave audio editing software http://www.goldwave.com. A visual target was a single 50 ms change in the brightness of the black background that could vary in brightness from 5% to 70% (black = 0% brightness, white = 100%). Eight different brightness gradations were created (5%, 10%, 20%, 30%, 40%, 50%, 60%, and 70% of a pure white background) using the lightness function in Photoshop http://www.adobe.com. These graded stimuli were designed to generate a task where participants would have to make present/absent judgments of various difficulty, not to measure precise signal detection properties of each stimulus intensity. The nature of the paradigm, using cues and varying levels of target intensities rather than streams of stimuli at regular intervals, ensures that no-target trials will not elicit an omitted stimulus response.
Experiments were performed on a 1.5T GE echo-speed Horizon LX scanner with a birdcage headcoil (GE Medical Systems). High-resolution T1-weighted structural scans were obtained using an inversion recovery 3D spoiled gradient echo sequence (matrix size: 256 × 256, field of view: 24 cm, slice thickness: 3 mm, 128 slices). Whole-brain activation was assessed by examining BOLD signal  alterations produced by the changes in blood oxygenation that accompany cortical activation. Functional images were acquired using multi-slice gradient-echo planar imaging (EPI; TR: 2100 ms, TE: 40 ms, matrix size: 64 × 64, slice thickness: 5 mm, 28 slices).
A measure of signal detectiblity, d', was calculated for each attention condition using the hit rate (% of trials where a subject correctly identified that a target was present) and the false alarm rate (% of trials where there was no target but the subject incorrectly responded that one was present), in the formula d' = Zfalse alarm - Zhit. Although d' analyses are typically performed to evaluate the detectibility of a stimulus of a single intensity, we used the analysis to compare our participants' sensitivity to a range of stimulus intensities across the different attention conditions, while controlling for participants' response biases. Thus our analyses should not be interpreted as a standard signal-detection experiment, but rather as a measure of participants' ability to detect any gradation of the auditory or visual stimuli during selective and divided attention.
The functional images from each subject were reconstructed and processed with SPM99 http://www.fil.ion.ucl.ac.uk/spm/software/spm99. Data sets were corrected for slice timing to accurately align images with the time course of the paradigm. To correct for motion, data sets were realigned using the first image as the reference. Images were then normalized to Montreal Neurological Institute space based on the EPI template in SPM99. Images were smoothed using a Gaussian kernel (full width at half maximum, 8 × 8 × 10 mm).
Statistical parametric maps were generated in SPM99 using the general linear model. A regression analysis was performed at each voxel to determine the parameter estimates for each trial type. Each trial in the paradigm was modeled as a single event and the time course of events was convolved with a canonical hemodynamic response function and the time derivative was included. Randomly presented rest trials provided a measure of baseline activity.
Data from the five task runs were combined for each subject in a fixed effects analysis. Contrast weights were applied to the parameter estimates for each trial type, in order to identify regions where the BOLD signal change was correlated with the stimulation paradigm. For example, to identify regions of increased activity during auditory attention trials, a +1 contrast weight was applied to the parameter estimate for that trial type and a 0 contrast weight was applied to all other trial types. Importantly, a -1 contrast weight applied to the parameter estimate for this trial type would identify regions of decreased activity during auditory attention trials. A contrast image representing the sum of the weighted parameter estimates was then generated for each effect of interest. The contrast images for each subject were then used to perform random effects group analyses, where activity between trial types could be compared (e.g., where was activity greater during auditory attention than during visual attention).
Data were globally normalized to allow for group comparisons using proportional scaling of image means and all statistical maps were thresholded at p < 0.001 and corrected for multiple comparisons using extent correction (p < 0.05) unless otherwise noted. In regions identified to have significantly greater activity during one attention condition than another, an ROI (10 mm sphere, centered on the peak voxel in the largest cluster of activation) was drawn to explore the effects driving the differences in activity between the attention conditions. The mean percent signal change in each ROI was then averaged across subjects and compared during each stimulus condition. One sample t-tests were used to determine if signal changes in these ROIs were significantly different from baseline during each stimulus condition, and 2 × 2 repeated measures ANOVAs were conducted to examine the impact of target (present or absent) and attended modality (audition or vision) on signal change in the auditory cortex and the visual cortex.
Average hit rate, false alarm rate, and detectibility (d') with standard deviations (SD) for each cue/target condition.
% false alarms
% false alarms
The subtle stimuli used as targets in this experiment did not produce large positive changes in the BOLD signal, so it is unlikely that they were the only factors driving the deactivations in unattended sensory cortices. However, the presence of the target in these trials does not allow the relative contributions of sensory- and attention-driven deactivations to be ascertained. Therefore, sensory responses to "no-target" trials were also analyzed.
In the auditory cortex, there was also a significant effect of attended modality (F1,14 = 24.80, p < 0.001), and no effect of target status (F1,14 = 0.26, ns), but there was a significant interaction of attention and target (F1,14 = 19.29, p < 0.001). This analysis demonstrates that there was less activity in the auditory cortex during visual attention than auditory attention, and that this activity (both activation during auditory attention and deactivation during visual attention) was reduced in magnitude in the absence of a target (Fig. 6B).
Attention is a neural mechanism for selecting behaviorally relevant information from the multitude of stimuli encountered in the environment. Data from psychophysical investigations suggest that the primary behavioral gains of modality-specific attention come from suppression of responses to stimuli in the unattended modality rather than enhancing responses to attended stimuli. Results of the present fMRI study seem to reflect the neural underpinnings of this phenomenon, as the primary difference between attending to vision and audition was decreased neural activity in the unattended sensory modality rather than enhancement of activity in the attended modality. Notably, this attentional modulation was also observed on trials when no target was presented following the attentional cue. Studies exploring visual spatial attention have demonstrated a similar effect, whereby simply directing attention to a particular location modulates sensory cortex activity, independent of stimulus presentation [14, 31].
Suppression of visual cortex during auditory attention was not diminished in the absence of a target; however, the magnitude of activity increases and decreases in the auditory cortex was reduced when no target was presented in the attended modality. Sub-threshold deactivations of auditory cortex were still noted during visual attention no-target trials, indicating that there may be an additive effect between top-down components of attention and bottom-up influences of sensory stimulation that occurs when a cue is followed by a target. Smaller deactivations in auditory cortex during the no- target conditions could reflect the absence of this additive effect. The visual stimulus used in this paradigm did not produce significant activation in the visual cortex; however, future experiments using more effective visual stimuli might allow the observation of increased stimulus-driven deactivations in the auditory cortex as well as activations in the visual cortex. Additionally, utilizing different visual stimuli would likely activate visual cortex regions not encompassed by the ROI analyzed in this experiment. Other regions of visual cortex may show different relationships between stimulus and attention-driven modulations.
An alternative explanation for reduced deactivations of auditory cortex during no-target conditions is that our experimental design required there to be fewer no-target trials than trials where the target is present, which may have reduced the detectibility of attention-mediated changes in activity that are independent of stimulus presentation. Future studies containing a greater proportion of no-target trials may shed further light onto this finding.
Our imaging results are in accord with data from behavioral studies demonstrating that modality-specific attention generally produces large behavioral decrements for tasks in the unattended sensory modality, but only small benefits for tasks in the attended modality [16, 21]. While our experimental design precluded the observation of behavioral decrements, we were able to measure small, but significant behavioral improvements associated with auditory attention. Future studies utilizing alternative experimental designs will be required to explore the neural events associated with behavioral performance decrements.
Importantly, however, the behavioral enhancements resulting from selective auditory attention were reflected in the neural activity changes observed in both auditory and visual cortices during auditory attention. Behavioral benefits of visual attention were only apparent in speeded response times, not enhanced detection, and the neural activity changes corresponding to visual attention are not as robust as those for auditory attention. One possible source of differences between results for the two modalities is that the visual and auditory environments in the MR scanner are somewhat disparate due to the acoustic noise generated by rapid gradient switching. Thus, when auditory stimuli were presented in the midst of ongoing scanner noise, increased selective attention may have been required. In contrast, when the visual stimuli were presented, there was little competing visual noise, possibly requiring less engagement of selective attention mechanisms. Another potential explanation for the divergence in auditory and visual results is that deactivations in the visual cortex observed in the absence of an auditory target could due to the continuous auditory noise in the scanner environment. That is, scanner noise could be acting as an ongoing auditory signal, producing deactivations in visual cortex indistinguishable from those produced by the auditory target tone used in this paradigm. To equate the visual and auditory environments more closely, future studies could use sparse or clustered temporal acquisition fMRI techniques to present auditory stimuli without the presence of background scanner noise .
In contrast to previous reports [18–21, 27], attention to a particular modality during our task did not increase activity in the attended sensory cortex. In each of these previous studies, however, a salient stimulus was always present in the attended modality. The stimuli used in our detection paradigm were, by necessity, often nearly imperceptible and, at times, completely absent. Thus the increases observed in the attended modality for previous studies were likely due to enhanced responses to attended stimuli, not increases in baseline activity in the attended modality.
Interactions between stimulus salience and attentional modulation of both attended and unattended sensory cortices are consistent with data from Shulman et al. (1997). They demonstrated that in paradigms producing a weak response to passive sensory stimulation, there was also little modulation during active attention to the same sensory stimuli. In contrast, robust attentional modulation of attended stimuli was observed for stimulus conditions that produced a strong sensory response during passive viewing . Rinne and colleagues (2005) also demonstrated an interaction between auditory stimulus presentation rate and attentional modulation. Increasing sound presentation rate and focusing attention on the auditory modality both increased auditory cortex activity, however, attentional effects are enhanced at higher sound presentation rates .
In summary, our data demonstrate that modality-specific selective attention produces activity decreases in the ignored sensory modality and not 'true' increases in cortical activity for the attended modality. These data are consistent with behavioral experiments demonstrating that performance enhancements during modality-specific selective attention result primarily from decreased processing in the unattended modality not increased processing in the attended modality. Furthermore, this experiment demonstrates that deactivations of cross-modal cortices noted during sensory stimulation can be produced exclusively by endogenous focusing of attention on the target modality and are not solely dependent on the presentation of a stimulus. However, the data suggest an additive effect of attentional and stimulus-driven effects. Activity increases in the attended modality have been previously reported when subjects are actively processing highly salient stimuli. In our work we did not see a significant increase in baseline activity in the attended modality, suggesting that activations in the attended modality are likely dependent on an interaction between attention and the presence of a salient stimulus. Such an interpretation of the effect of modality-specific selective attention is reasonable given that there would be no behavioral benefit of increasing background activity in the absence of a stimulus, but there would be a benefit of enhancing a response to a particular stimulus.
This work was supported by an NIH grant (K08 NS42568) to PJL.
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