Alpha band oscillations track temporal orienting of attention

Introduction: Recent investigations using field-potential recordings in visual and auditory cortices have shown that oscillatory activity in neuronal ensembles become entrained to the timing of rhythmically presented stimuli according to their modality and location (Lakatos, Chen et al. 2007; Lakatos, Karmos et al. 2008; Lakatos, O'Connell et al. 2009). In spite of the evidence showing the role of brain oscillations on forming predictions about forthcoming sensory events (for a review (Engel, Fries et al. 2001), little is known about the role of such oscillations in the temporal orienting of attention (Nobre 2001; Coull and Nobre 2008). To test the effect of temporal orienting of attention on early perceptual processing, motor selection, and anticipatory low frequency oscillation (alpha waves), we analysed EEG data from healthy adults participants who were performing a visual perceptual discrimination task of targets preceded by rhythmic spatio-temporal cues.

Methods: EEG was recorded continuously from 30 healthy, right-handed participants [mean age, 23.9 years (SD, 4.9 years); range, 19–32 years; 9 males], using a 34 Ag/AgCl electrodes at 1000Hz (AFZ ground, right mastoid reference) in an electrically shielded room. The task consisted of rhythmic stimuli that cued participants to the time and location that a subsequent target stimulus would occur after an occlusion (Fig. 1). At the beginning of each trial, a stimulus (ball - diameter:1.0°) appeared on the upper (50%) or lower (50%) left side of the screen and moved across the screen in a diagonal spatial trajectory of seven steps (200 ms for each step). Temporal orienting was induced by manipulating the SOA of each stimuli in three different conditions: fast (400 ms), slow (800 ms) and neutral, where the SOA within a trial was unpredictable, and varied randomly between 300-900 ms. Upon reaching an “occluder”, the ball disappeared for 600 (short occlusion) or 1400ms (long occlusion). When it reappeared on the right-hand side of the occluder, it contained an upright or tilted cross (200 ms, for which participants were required to discriminate the target, using a button-press response with either their right or left hand accordingly. The time-frequency analysis was performed in unfiltered continuous data, epoched from -700 to 1800 ms relative to the beginning of the occlusion period. Data from 12 participants had to be excluded from the analysis due to excessive artifacts in the EEG recordings or poor behavioural performance (accuracy < 60%). A multitaper time–frequency transformation was applied to all electrodes in each trial. This transformation produced an estimation of oscillatory power for each time sample and frequencies between 4 and 20 Hz. Alpha power (8 to 14 Hz) values were extracted from the epochs and submitted to a repeated-measures. All frequency analysis was done using Fieldtrip package ("http://www.ru.nl/fcdonders/fieldtrip/":http://www.ru.nl/fcdonders/fieldtrip/) for MATLAB (MatWorks).

Results: To test the effect of reorienting of attention in time we analyzed alpha band oscillations during the long occlusion period. In this way we can observed the reorienting effect in the invalid (fast) trials, when participants have to shift their attention to the long occlusion given that the target did not appear after the expected cued (short) interval. This result reveals an alpha desynchronization preceding the expected target (blue dashed line). When comparing these oscillations within the same period for the slow (valid) rhythm, we observed that this desynchronization in alpha is only present when preceding by a fast, but not slow, rhythm [F(1,17) = 3.85; p = 0.029]. As can be observed in Figure 2, in the valid condition (slow rhythm) there is also a desynchronization of alpha preceding the cued late target. However, if we compare the alpha oscillations preceding the appearance of the later presented target for the valid and invalid temporal cues, no significant difference is observed [F(1,17) = 0.31; p = 0.905]. 
 
Conclusion: Our findings support the hypothesis that temporal orienting can also modulate brain oscillations, specifically in the alpha range. Importantly, we showed that in the invalid (fast) condition, in which participants were prepared for a target presentation after a short occlusion, there was also a preparation for the presentation of the later target. This indicates that participants were able to reorient their attention to the second interval given that the target fail to appear after the short (expected) occlusion.

References:
Coull, J. and A. Nobre (2008). "Dissociating explicit timing from temporal expectation with fMRI." _Current Opinion in Neurobiology_ 18(2): 137-44.
Engel, A. K., P. Fries, et al. (2001). "Dynamic predictions: oscillations and synchrony in top-down processing." _Nature Reviews Neuroscience_ 2(10): 704-16.
Lakatos, P., C. M. Chen, et al. (2007). "Neuronal oscillations and multisensory interaction in primary auditory cortex." _Neuron_ 53(2): 279-92.
Lakatos, P., G. Karmos, et al. (2008). "Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection." _Science_ 320(5872): 110-113.
Lakatos, P., M. N. O'Connell, et al. (2009). "The leading sense: supramodal control of neurophysiological context by attention." _Neuron_ 64(3): 419-30.
Nobre, A. C. (2001). "Orienting attention to instants in time." _Neuropsychologia_ 39(12): 1317-28.
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Behavioural Dissociation between Exogenous and Endogenous Temporal Orienting of Attention

BACKGROUND: In the current study we compared the effects of temporal orienting of attention based on predictions carried by the intrinsic temporal structure of events (rhythm) and by instructive symbolic cues; and tested the degree of cognitive, strategic control that could be exerted over each type of temporal expectation. The experiments tested whether the distinction between exogenous and endogenous orienting made in spatial attention may extend to the temporal domain. TASK DESIGN AND MAIN RESULTS: In this task, a ball moved across the screen in discrete steps and disappeared temporarily under an occluding band. Participants were required to make a perceptual discrimination on the target upon its reappearance. The regularity of the speed (rhythmic cue) or colour (symbolic cue) of the moving stimulus could predict the exact time at which a target would reappear after a brief occlusion (valid trials) or provide no temporal information (neutral trials). The predictive nature of rhythmic and symbolic cues was manipulated factorially in a symmetrical and orthogonal fashion. To test for the effects of strategic control over temporal orienting based on rhythmic or symbolic cues, participants were instructed either to "attend-to-speed" (rhythm) or "attend-to-colour". Our results indicated that both rhythmic and symbolic (colour) cues speeded reaction times in an independent fashion. However, whilst the rhythmic cueing effects were impervious to instruction, the effects of symbolic cues were contingent on the instruction to attend to colour. FINAL CONCLUSIONS: Taken together, our results provide evidence for the existence of qualitatively separable types of temporal orienting of attention, akin to exogenous and endogenous mechanisms

Temporal orienting in the human brain: neural mechanisms of control and modulation

The main aim of the experiments reported in this thesis was to explore the neural mechanisms underlying the temporal orienting of attention. In Chapter 3, I explored the possible dissociation between exogenous and endogenous temporal orienting by comparing reaction times to targets appearing after rhythmic or symbolic cues. Behavioural results provided evidence for the existence of dissociable exogenous and endogenous types of temporal orienting of attention. The experiment in Chapter 4 combined spatiotemporal expectations using rhythmic moving cues to test the modulatory effect of exogenous temporal orienting in the brain. Specifically, I used EEG to test the effect of temporal orienting on perceptual and motor stages of target analysis, as well as on anticipatory oscillatory brain activity. The time-frequency analysis revealed that rhythmic cues can entrain slow brains oscillations, providing a putative mechanism for enhancing the perceptual processing of expected events. Spatiotemporal expectations also modulated the amplitude of visual responses and the timing and amount of preparatory motor activity. In Chapter 5, I used a novel task to explore the neural modulatory effects of spatial and temporal expectations acting in isolation or in coordination. For the first time, the analysis of early visual responses demonstrated that temporal expectations alone, independently of spatial orienting, can enhance early visual perceptual processes. The time-frequency analysis in this experiment showed a desynchronisation of alpha oscillations focused over central-parietal electrodes induced by rhythmic cues that were independent of spatial expectations. When rhythmic cues carried spatiotemporal information, the alpha desynchronisation also spread over contralateral occipital electrodes. In Chapter 6, fMRI was used to test the possible neural dissociation between motor and temporal orienting. The results confirmed the large overlap between these two processes, but also indicated independent behavioural and neural effects of temporal orienting. Temporal orienting activated the left IPS across motor conditions, further implicating the left IPS in temporal orienting. Based on the results of these experiments, directions for future studies are discussed.Some sections of this thesis have been removed from dissemination due to copyright reasons

Performance modulations phase-locked to action depend on internal state

Several studies have probed perceptual performance at different times after a self-paced motor action and found frequency-specific modulations of perceptual performance phase-locked to the action. Such action-related modulation has been reported for various frequencies and modulation strengths. In an attempt to establish a basic effect at the population level, we had a relatively large number of participants (n=50) perform a self-paced button press followed by a detection task at threshold, and we applied both fixed- and random-effects tests. The combined data of all trials and participants surprisingly did not show any significant action-related modulation. However, based on previous studies, we explored the possibility that such modulation depends on the participant’s internal state. Indeed, when we split trials based on performance in neighboring trials, then trials in periods of low performance showed an action-related modulation at ≈17 Hz. When we split trials based on the performance in the preceding trial, we found that trials following a “miss” showed an action-related modulation at ≈17 Hz. Finally, when we split participants based on their false-alarm rate, we found that participants with no false alarms showed an action-related modulation at ≈17 Hz. All these effects were significant in random-effects tests, supporting an inference on the population. Together, these findings indicate that action-related modulations are not always detectable. However, the results suggest that specific internal states such as lower attentional engagement and/or higher decision criterion are characterized by a modulation in the beta-frequency range