We investigated the effects of spatial-selective attention on oscillatory neuronal dynamics in a tactile delayed-match-to-sample task. Whole-head magnetoencephalography was recorded in healthy subjects while dot patterns were presented to their index fingers using Braille stimulators. The subjects' task was to report the reoccurrence of an initially presented sample pattern in a series of up to eight test stimuli that were presented unpredictably to their right or left index finger. Attention was cued to one side (finger) at the beginning of each trial, and subjects performed the task at the attended side, ignoring the unattended side.After stimulation, high-frequency gamma-band activity (60 -95 Hz) in presumed primary somatosensory cortex (S1) was enhanced, whereas alpha-and beta-band activity were suppressed in somatosensory and occipital areas and then rebounded. Interestingly, despite the absence of any visual stimulation, we also found time-locked activation of medial occipital, presumably visual, cortex. Most relevant, spatial tactile attention enhanced stimulus-induced gamma-band activity in brain regions consistent with contralateral S1 and deepened and prolonged the stimulus induced suppression of beta-and alpha-band activity, maximal in parieto-occipital cortex. Additionally, the beta rebound over contralateral sensorimotor areas was suppressed.We hypothesize that spatial-selective attention enhances the saliency of sensory representations by synchronizing neuronal responses in early somatosensory cortex and thereby enhancing their impact on downstream areas and facilitating interareal processing. Furthermore, processing of tactile patterns also seems to recruit visual cortex and this even more so for attended compared with unattended stimuli.
The brain adapts to dynamic environments by adjusting the attentional gain or precision afforded to salient and predictable sensory input. Previous research suggests that this involves the regulation of cortical excitability (reflected in prestimulus alpha oscillations) before stimulus onset that modulates subsequent stimulus processing (reflected in stimulus-bound gamma oscillations). We present two spatial attention experiments in humans, where we first replicate the classic finding of prestimulus attentional alpha modulation and poststimulus gamma modulation.Inthesecondexperiment,thetask-relevanttargetwasastimuluschangethatoccurredafterstimulusonset.Thisenabledustoshow that attentional alpha modulation reflects the predictability (precision) of an upcoming sensory target, rather than an attenuation of alpha activity induced by neuronal excitation related to stimulus onset. In particular, we show that the strength of attentional alpha modulations increases with the predictability of the anticipated sensory target, regardless of current afferent drive. By contrast, we show that the poststimulus attentional gamma enhancement is stimulus-bound and decreases when the subsequent target becomes more predictable. Hence, this pattern suggests that the strength of gamma oscillations is not merely a function of cortical excitability, but also depends on the relative mismatch of predictions and sensory evidence. Together, these findings support recent theoretical proposals for distinct roles of alpha/beta and gamma oscillations in hierarchical perceptual inference and predictive coding.
A person's ability to detect a weak visual target stimulus varies from one viewing to the next. We tested whether the trial-to-trial fluctuations of neural population activity in the human brain are related to the fluctuations of behavioral performance in a "yes-no" visual motion-detection task. We recorded neural population activity with whole head magnetoencephalography (MEG) while subjects searched for a weak coherent motion signal embedded in spatiotemporal noise. We found that, during motion viewing, MEG activity in the 12- to 24-Hz ("beta") frequency range is higher, on average, before correct behavioral choices than before errors and that it predicts correct choices on a trial-by-trial basis. This performance-predictive activity is not evident in the prestimulus baseline and builds up slowly after stimulus onset. Source reconstruction revealed that the performance-predictive activity is expressed in the posterior parietal and dorsolateral prefrontal cortices and, less strongly, in the visual motion-sensitive area MT+. The 12- to 24-Hz activity in these key stages of the human dorsal visual pathway is correlated with behavioral choice in both target-present and target-absent conditions. Importantly, in the absence of the target, 12- to 24-Hz activity tends to be higher before "no" choices ("correct rejects") than before "yes" choices ("false alarms"). It thus predicts the accuracy, and not the content, of subjects' upcoming perceptual reports. We conclude that beta band activity in the human dorsal visual pathway indexes, and potentially controls, the efficiency of neural computations underlying simple perceptual decisions.
Inferring the environment's statistical structure and adapting behavior accordingly is a fundamental modus operandi of the brain. A simple form of this faculty based on spatial attentional orienting can be studied with Posner's location-cueing paradigm in which a cue indicates the target location with a known probability. The present study focuses on a more complex version of this task, where probabilistic context (percentage of cue validity) changes unpredictably over time, thereby creating a volatile environment. Saccadic response speed (RS) was recorded in 15 subjects and used to estimate subject-specific parameters of a Bayesian learning scheme modeling the subjects' trial-by-trial updates of beliefs. Different response models—specifying how computational states translate into observable behavior—were compared using Bayesian model selection. Saccadic RS was most plausibly explained as a function of the precision of the belief about the causes of sensory input. This finding is in accordance with current Bayesian theories of brain function, and specifically with the proposal that spatial attention is mediated by a precision-dependent gain modulation of sensory input. Our results provide empirical support for precision-dependent changes in beliefs about saccade target locations and motivate future neuroimaging and neuropharmacological studies of how Bayesian inference may determine spatial attention.
SummaryCognitive processes such as visual perception and selective attention induce specific patterns of brain oscillations [1–6]. The neurochemical bases of these spectral changes in neural activity are largely unknown, but neuromodulators are thought to regulate processing [7–9]. The cholinergic system is linked to attentional function in vivo [10–13], whereas separate in vitro studies show that cholinergic agonists induce high-frequency oscillations in slice preparations [14–16]. This has led to theoretical proposals [17–19] that cholinergic enhancement of visual attention might operate via gamma oscillations in visual cortex, although low-frequency alpha/beta modulation may also play a key role. Here we used MEG to record cortical oscillations in the context of administration of a cholinergic agonist (physostigmine) during a spatial visual attention task in humans. This cholinergic agonist enhanced spatial attention effects on low-frequency alpha/beta oscillations in visual cortex, an effect correlating with a drug-induced speeding of performance. By contrast, the cholinergic agonist did not alter high-frequency gamma oscillations in visual cortex. Thus, our findings show that cholinergic neuromodulation enhances attentional selection via an impact on oscillatory synchrony in visual cortex, for low rather than high frequencies. We discuss this dissociation between high- and low-frequency oscillations in relation to proposals that lower-frequency oscillations are generated by feedback pathways within visual cortex [20, 21].
Selective attention allows us to focus on particular sensory modalities and locations. Relatively little is known about how attention to a sensory modality may relate to selection of other features, such as spatial location, in terms of brain oscillations, although it has been proposed that low-frequency modulation (α- and β-bands) may be key. Here, we investigated how attention to space (left or right) and attention to modality (vision or touch) affect ongoing low-frequency oscillatory brain activity over human sensory cortex. Magnetoencephalography was recorded while participants performed a visual or tactile task. In different blocks, touch or vision was task-relevant, whereas spatial attention was cued to the left or right on each trial. Attending to one or other modality suppressed α-oscillations over the corresponding sensory cortex. Spatial attention led to reduced α-oscillations over both sensorimotor and occipital cortex contralateral to the attended location in the cue-target interval, when either modality was task-relevant. Even modality-selective sensors also showed spatial-attention effects for both modalities. The visual and sensorimotor results were generally highly convergent, yet, although attention effects in occipital cortex were dominant in the α-band, in sensorimotor cortex, these were also clearly present in the β-band. These results extend previous findings that spatial attention can operate in a multimodal fashion and indicate that attention to space and modality both rely on similar mechanisms that modulate low-frequency oscillations.
Correlative evidence provides support for the idea that brain oscillations underpin neural computations. Recent work using rhythmic stimulation techniques in humans provide causal evidence but the interactions of these external signals with intrinsic rhythmicity remain unclear. Here, we show that sensorimotor cortex follows externally applied rhythmic TMS (rTMS) stimulation in the beta-band but that the elicited responses are strongest at the intrinsic individual beta peak frequency. While these entrainment effects are of short duration, even subthreshold rTMS pulses propagate through the network and elicit significant cortico-spinal coupling, particularly when stimulated at the individual beta-frequency.Our results show that externally enforced rhythmicity interacts with intrinsic brain rhythms such that the individual peak frequency determines the effect of rTMS. The observed downstream spinal effect at the resonance frequency provides evidence for the causal role of brain rhythms for signal propagation.
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