F.L. van Ede

Prior Expectation Mediates Neural Adaptation to Repeated Sounds in the Auditory Cortex: An MEG Study

Repetition suppression, the phenomenon that the second presentation of a stimulus attenuates neural activity, is typically viewed as an automatic consequence of repeated stimulus presentation. However, a recent neuroimaging study has suggested that repetition suppression may be driven by top-down expectations. Here we examined whether and when repetition suppression can be modulated by top-down expectation. Participants listened to auditory stimuli in blocks where tone repetitions were either expected or unexpected, while we recorded ongoing neural activity using magnetoencephalography. We found robust repetition suppression in the auditory cortex for repeated tones. Interestingly, this reduction was significantly larger for expected than unexpected repetitions, both in terms of evoked activity and gamma-band synchrony. These findings indicate a role of top-down expectation in generating repetition suppression and are in line with predictive coding models of perception, in which the difference between expected and actual input is propagated from lower to higher cortical areas.

Orienting Attention to an Upcoming Tactile Event Involves a Spatially and Temporally Specific Modulation of Sensorimotor Alpha- and Beta-Band Oscillations

Our perception is facilitated if we know where and when a sensory stimulus will occur. This phenomenon is accounted for by spatial and temporal orienting of attention. Whereas spatial orienting of attention has repeatedly been shown to involve spatially specific modulations of ongoing oscillations within sensory cortex, it is not clear to what extent anticipatory modulations of ongoing oscillations are involved in temporal orienting of attention. To address this, we recorded magnetoencephalography while human participants performed a tactile discrimination task. We cued participants to the left or the right hand, after which a tactile stimulus was presented at one of several fixed temporal delays. We thus assessed whether and how ongoing sensorimotor oscillations are modulated during tactile anticipation. We provide evidence for three phenomena. First, orienting to an upcoming tactile event involves a spatially specific contralateral suppression of alpha- and beta-band oscillations within sensorimotor cortex. Second, this modulation is deployed with temporal specificity, and this is more pronounced for beta-band compared with alpha-band oscillations. Third, the contralateral suppression of beta-band oscillations is associated with faster responses to subsequently presented tactile stimuli. Control measures showed that these results cannot be explained by motor planning or execution. We conclude that the modulation of ongoing oscillations within sensory cortex reflects a unifying mechanism underlying both spatial and temporal orienting of attention.

Tactile expectation modulates pre-stimulus beta-band oscillations in human sensorimotor cortex

Neuronal oscillations are postulated to play a fundamental role in top-down processes of expectation. We used magnetoencephalography (MEG) to investigate whether expectation of a tactile event involves a pre-stimulus modulation of neuronal oscillations in human somatosensory cortex. In a bimodal attention paradigm, participants were presented with a predictable spatio-temporal pattern of lateralized tactile stimulations and simultaneously occurring non-lateralized auditory stimuli. Before the onset of a series of such combined audio-tactile stimuli, a cue was presented that indicated the sensory stream that had to be attended. By investigating lateralized patterns of oscillatory activity, we were able to study both attentive (when the tactile stream was attended) and non-attentive (when the auditory stream was attended) tactile expectations. For both attention conditions, we observed a lateralized modulation of the amplitude of beta band oscillations prior to a predictable - and accordingly lateralized - tactile stimulus. As such, we show that anticipatory modulation of ongoing oscillatory activity is not restricted to attended sensory events. Attention did enlarge the size of this modulation. We argue that this modulation constitutes a suppression of beta oscillations that originate at least partly from primary somatosensory cortex (S1) contralateral to the expected stimulation. We discuss our results in the light of the hypothesis that ongoing beta oscillations over sensorimotor cortex reflect a brain state in which neuronal processing efficacy is low. Pre-stimulus suppression of these oscillations then prepares the system for future processing. This shows that perception is an active process that starts even prior to sensation.

Attentional Cues Affect Accuracy and Reaction Time via Different Cognitive and Neural Processes

We investigated whether symbolic endogenous attentional cues affect perceptual accuracy and reaction time (RT) via different cognitive and neural processes. We recorded magnetoencephalography in 19 humans while they performed a cued somatosensory discrimination task in which the cue–target interval was varied between 0 and 1000 ms. Comparing behavioral and neural measures, we show that (1) attentional cueing affects accuracy and RT with different time courses and (2) the time course of our neural measure (anticipatory suppression of neuronal oscillations in stimulus-receiving sensory cortex) only accounts for the accuracy time course. A model is proposed in which the effect on accuracy is explained by a single process (preparatory excitability increase in sensory cortex), whereas the effect on RT is explained by an additional process that is sensitive to cue–target compatibility (post-target comparison between expected and actual stimulus location). These data provide new insights into the mechanisms underlying behavioral consequences of attentional cueing.

Diverse phase relations among neuronal rhythms and their potential function

Neuronal oscillations at nearby sites in the brain often show phase relations that are consistent across time, yet diverse across space. We discuss recent demonstrations of this phase relation diversity, and show that, contrary to earlier beliefs, this diversity is a general property of oscillations that is neither restricted to low-frequency oscillations nor to periods outside of stimulus processing. Arguing for the computational relevance of phase relation diversity, we discuss that it can be modulated by sensory and motor events, and put forward the idea that phase relation diversity may support effective neuronal communication by (i) enhancing selectivity and (ii) allowing for the concurrent segregation of multiple information streams.

Attentional modulations of somatosensory alpha, beta and gamma oscillations dissociate between anticipation and stimulus processing

What are the spectral signatures of somatosensory attention? Here we show that the answer to this question depends critically on the sensory context in which attention is deployed. We recorded magnetoencephalography (MEG) in humans and investigated tactile spatial attention in two different sensory contexts: in anticipation and during the processing of sustained tactile stimuli. We observe a double dissociation between these contexts and two key electrophysiological correlates of attention: in anticipation we primarily observe an attentional suppression of contralateral alpha and beta oscillations (8-12 and 15-30 Hz, respectively), whereas during stimulus processing we primarily observe an attentional amplification of contralateral gamma oscillations (55-75 Hz). This dissociation is well explained by the different neural states that occur prior and during the stimulus, and on which attention can exert its influence. In line with analogous observations in the visual modality, this suggests that the neural implementation of attention must be understood in relation to context and existing brain states. Consequently, different signatures of attention may contribute to perception in different contexts and, as our data reveals for the attentional modulation of alpha oscillations, these are not always required for attention to improve perception. At the same time, these data demonstrate that the attentional modulations of alpha and gamma oscillations (during, respectively, attentional orienting and attentional selection), are generalizable phenomena across the different sensory modalities.

Beyond establishing involvement: quantifying the contribution of anticipatory α- and β-band suppression to perceptual improvement with attention.

Systems and cognitive neuroscience aim at understanding the neurophysiological mechanisms that underlie cognition and behavior. Many studies have revealed the involvement of many types of neural signals in diverse cognitive and behavioral phenomena. Here, we go beyond establishing such involvement and address two fundamental, yet largely unaddressed, questions: 1) exactly how much does a given neural signal contribute to a cognitive or behavioral phenomenon of interest; and 2) to what extent are distinct neural signals independently related to this phenomenon? We recorded brain activity using magnetoencephalography while human participants performed a cued somatosensory detection task. Using a novel method, we then quantified the contribution (in a predictive but not causal sense) of two well-established neural phenomena to the improvement in perception with attentional orienting. In our sample, the anticipatory suppression of extracranially recorded oscillatory α- and β-band amplitudes from contralateral primary somatosensory cortex could account for maximally 29% of the attention-induced improvement in tactile perception. In addition, although amplitude suppressions in the α- and β-frequency bands both contributed to this improvement, their contribution was largely shared. These data reveal the upper limit of the cognitive/behavioral relevance of this type of signal and show that at least 71% of the perceptual improvement with attention must be accounted for by other signals.

Somatosensory Demands Modulate Muscular Beta Oscillations, Independent of Motor Demands

Neural oscillations in the beta band (15–30 Hz) occur coherently throughout the primate somatomotor network, comprising somatomotor cortices, basal ganglia, thalamus, cerebellum, and spinal cord, with the latter resulting in beta oscillations in muscular activity. In accordance with the anatomy of this network, these oscillations have traditionally been associated strictly with motor function. Here we show in humans that somatosensory demands, both in anticipation and during the processing of tactile stimuli, also modulate beta oscillations throughout this network. Specifically, somatosensory demands suppress the degree to which not only cortical activity but also muscular activity oscillates in the beta band. This suppression of muscular beta oscillations by perceptual demands is specific to demands in the somatosensory modality and occurs independent of movement preparation and execution: it occurs even when no movement is required at all. This places touch perception as an important computation within this widely distributed somatomotor beta network and suggests that, at least in healthy subjects, somatosensation and action should not be considered as separable processes, not even at the level of the muscles.

Driving Human Motor Cortical Oscillations Leads to Behaviorally Relevant Changes in Local GABAA Inhibition: A tACS-TMS Study.

Beta and gamma oscillations are the dominant oscillatory activity in the human motor cortex (M1). However, their physiological basis and precise functional significance remain poorly understood. Here, we used transcranial magnetic stimulation (TMS) to examine the physiological basis and behavioral relevance of driving beta and gamma oscillatory activity in the human M1 using transcranial alternating current stimulation (tACS). tACS was applied using a sham-controlled crossover design at individualized intensity for 20 min and TMS was performed at rest (before, during, and after tACS) and during movement preparation (before and after tACS). We demonstrated that driving gamma frequency oscillations using tACS led to a significant, duration-dependent decrease in local resting-state GABAA inhibition, as quantified by short interval intracortical inhibition. The magnitude of this effect was positively correlated with the magnitude of GABAA decrease during movement preparation, when gamma activity in motor circuitry is known to increase. In addition, gamma tACS-induced change in GABAA inhibition was closely related to performance in a motor learning task such that subjects who demonstrated a greater increase in GABAA inhibition also showed faster short-term learning. The findings presented here contribute to our understanding of the neurophysiological basis of motor rhythms and suggest that tACS may have similar physiological effects to endogenously driven local oscillatory activity. Moreover, the ability to modulate local interneuronal circuits by tACS in a behaviorally relevant manner provides a basis for tACS as a putative therapeutic intervention. SIGNIFICANCE STATEMENT Gamma oscillations have a vital role in motor control. Using a combined tACS-TMS approach, we demonstrate that driving gamma frequency oscillations modulates GABAA inhibition in the human motor cortex. Moreover, there is a clear relationship between the change in magnitude of GABAA inhibition induced by tACS and the magnitude of GABAA inhibition observed during task-related synchronization of oscillations in inhibitory interneuronal circuits, supporting the hypothesis that tACS engages endogenous oscillatory circuits. We also show that an individuals physiological response to tACS is closely related to their ability to learn a motor task. These findings contribute to our understanding of the neurophysiological basis of motor rhythms and their behavioral relevance and offer the possibility of developing tACS as a therapeutic tool.

Anticipated moments: temporal structure in attention.

We have come to recognize the brain as a predictive organ, anticipating attributes of the incoming sensory stimulation to guide perception and action in the service of adaptive behaviour. In the quest to understand the neural bases of the modulatory prospective signals that prioritize and select relevant events during perception, one fundamental dimension has until recently been largely overlooked: time. In this Review, we introduce the burgeoning field of temporal attention and illustrate how the brain makes use of various forms of temporal regularities in the environment to guide adaptive behaviour and influence neural processing.