Cued Spatial Attention Drives Functionally Relevant Modulation of the Mu Rhythm in Primary Somatosensory Cortex

102

Despite recent advances in uncovering the neural signature of tactile working memory processing in animals and humans, the representation of internally modified somatosensory working memory content has not been studied so far. Here, recording EEG in human participants (n = 25) performing a modified delayed match-to-sample task allowed us to disambiguate internally driven memory processing from encoding-related delay activity. After presentation of two distinct vibrotactile frequencies to different index fingers, a visual cue indicated which of the two previous stimuli had to be maintained in working memory throughout a retention interval for subsequent frequency discrimination against a probe stimulus. During cued stimulus maintenance, α activity (8-13 Hz) over early somatosensory cortices was lateralized according to the cued tactile stimulus, even though the location of the stimuli was task irrelevant. The task-relevant memory content, in contrast, was found to be represented in right prefrontal cortex. The key finding was that the visually presented instructions triggered systematic modulations of prefrontal β-band activity (20-25 Hz), which selectively reflected the to-be-maintained frequency of the cued tactile vibration. The results expand previous evidence for parametric representations of vibrotactile frequency in the prefrontal cortex and corroborate a central role of dynamic β-band synchronization during active processing of an analog stimulus quantity in human working memory. In particular, our findings suggest that such processing supports not only sustained maintenance but also purposeful modification and updating of the task-relevant working memory contents.W orking memory (WM) refers to a set of operations necessary for maintenance and online processing of information in the service of behavior (1). Across primate species, and for most different types of to-be-maintained information, central WM function has been attributed to the lateral prefrontal cortex (PFC), but the precise nature of prefrontal contributions to stimulus maintenance is still discussed (for reviews, see refs. 2 and 3). Significant progress in delineating the neural signature of maintenance processing in the PFC has been achieved in the somatosensory domain using vibrotactile stimuli in delayed match-to-sample (DMTS) frequency-discrimination tasks. During frequency maintenance, single-cell firing (4) and neuronal population activity (5) in the inferior PFC of monkeys varies parametrically as a monotonic function of the to-be-maintained frequency. PFC engagement during vibrotactile DMTS maintenance also has been demonstrated in humans by task-related changes in hemodynamic responses (6) and synchronized oscillatory EEG/magnetoencephalographic (MEG) activity (7,8). In particular, using EEG, it was found recently that the amplitude of prefrontal oscillatory activity in the upper β band (20-25 Hz) increased linearly with the frequency of the previously presented vibration (8). Such a correlate of parametric † WM (4) in human EEG open...

Section: Discussioncontrasting

confidence: 57%

Section: Discussionmentioning

confidence: 91%

Stimulus-dependent EEG activity reflects internal updating of tactile working memory in humans

Spitzer

Blankenburg

2011

102

“…In support of this idea, several studies on visual perception have shown that anticipatory α-activity reflects the orienting of attention (9)(10)(11)(12)(13)(14) and influences detection performance (15)(16)(17). Recently, it was shown that the functionality of α-oscillations can be generalized to the somatosensory system (18)(19)(20)(21). Furthermore, α-activity has been implicated in visual (22)(23)(24)(25), auditory (26), and somatosensory working-memory performance (27).…”

mentioning

confidence: 88%

α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking

Haegens

Nácher

Luna

et al. 2011

678

627

Extensive work in humans using magneto-and electroencephalography strongly suggests that decreased oscillatory α-activity (8-14 Hz) facilitates processing in a given region, whereas increased α-activity serves to actively suppress irrelevant or interfering processing. However, little work has been done to understand how α-activity is linked to neuronal firing. Here, we simultaneously recorded local field potentials and spikes from somatosensory, premotor, and motor regions while a trained monkey performed a vibrotactile discrimination task. In the local field potentials we observed strong activity in the α-band, which decreased in the sensorimotor regions during the discrimination task. This α-power decrease predicted better discrimination performance. Furthermore, the α-oscillations demonstrated a rhythmic relation with the spiking, such that firing was highest at the trough of the α-cycle. Firing rates increased with a decrease in α-power. These findings suggest that α-oscillations exercise a strong inhibitory influence on both spike timing and firing rate. Thus, the pulsed inhibition by α-oscillations plays an important functional role in the extended sensorimotor system.T he prominent posterior α-rhythm (8-14 Hz) was first described by Hans Berger (1) and long considered to reflect cortical idling (2, 3). To a large extent, the α-rhythm has been ignored by animal neurophysiologists (but see ref. 4) and considered to be of little functional relevance. Thus, it remains largely unknown how ongoing α-oscillations relate to neuronal firing.In contrast to the idling hypothesis, converging electrophysiological evidence in humans suggests that α-oscillations play an important functional role in cognitive processing (5-7). In particular, α-activity might serve to shape the state of sensory brain regions to direct the flow of information and optimize performance (8). In support of this idea, several studies on visual perception have shown that anticipatory α-activity reflects the orienting of attention (9-14) and influences detection performance (15-17). Recently, it was shown that the functionality of α-oscillations can be generalized to the somatosensory system (18-21). Furthermore, α-activity has been implicated in visual (22-25), auditory (26), and somatosensory working-memory performance (27).These studies strongly suggest that decreased α-activity facilitates processing in task-relevant brain regions, whereas increased α-activity functions to suppress distracting input in task-irrelevant regions. However, given the strong oscillatory nature of the α-activity, it is less clear how it influences processing in a phasic manner. It has been suggested that α-oscillations serve to depress processing every ∼100 ms by a mechanism of pulsed inhibition (5,(28)(29)(30). In support of this notion, it has recently been demonstrated that perception is modulated by the prestimulus phase of the α-rhythm (31, 32). Likewise, it was recently shown that the magnitude of the blood-oxygen level-dependent signal in response to a visual...

“…They are found with magnetoencephalography (MEG) (1-4), EEG (5, 6), and local field potential (LFP) recordings from neocortex (7-9) and are preserved across species (10). Local beta oscillations and their coordination between regions are implicated in numerous functions, including sensory perception, selective attention, and motor planning and initiation (2,3,6,7,9,(11)(12)(13)(14)(15). Neocortical beta oscillations are disrupted in various neuropathologies, most notably Parkinson's disease (PD), in which treatments that alleviate motor symptoms also reverse the neocortical beta disruption (16,17).…”

mentioning

confidence: 99%

“…beta rhythm | magnetoencephalography | computational modeling | sensorimotor processing | Parkinson's disease B eta band rhythms (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29) are a commonly observed activity pattern in the brain. They are found with magnetoencephalography (MEG) (1)(2)(3)(4), EEG (5,6), and local field potential (LFP) recordings from neocortex (7)(8)(9) and are preserved across species (10). Local beta oscillations and their coordination between regions are implicated in numerous functions, including sensory perception, selective attention, and motor planning and initiation (2,3,6,7,9,(11)(12)(13)(14)(15).…”

mentioning

confidence: 99%

Neural mechanisms of transient neocortical beta rhythms: Converging evidence from humans, computational modeling, monkeys, and mice

Sherman

Lee

Law

et al. 2016

398

510

Human neocortical 15-29-Hz beta oscillations are strong predictors of perceptual and motor performance. However, the mechanistic origin of beta in vivo is unknown, hindering understanding of its functional role. Combining human magnetoencephalography (MEG), computational modeling, and laminar recordings in animals, we present a new theory that accounts for the origin of spontaneous neocortical beta. In our MEG data, spontaneous beta activity from somatosensory and frontal cortex emerged as noncontinuous beta events typically lasting <150 ms with a stereotypical waveform. Computational modeling uniquely designed to infer the electrical currents underlying these signals showed that beta events could emerge from the integration of nearly synchronous bursts of excitatory synaptic drive targeting proximal and distal dendrites of pyramidal neurons, where the defining feature of a beta event was a strong distal drive that lasted one beta period (∼50 ms). This beta mechanism rigorously accounted for the beta event profiles; several other mechanisms did not. The spatial location of synaptic drive in the model to supragranular and infragranular layers was critical to the emergence of beta events and led to the prediction that beta events should be associated with a specific laminar current profile. Laminar recordings in somatosensory neocortex from anesthetized mice and awake monkeys supported these predictions, suggesting this beta mechanism is conserved across species and recording modalities. These findings make several predictions about optimal states for perceptual and motor performance and guide causal interventions to modulate beta for optimal function. beta rhythm | magnetoencephalography | computational modeling | sensorimotor processing | Parkinson's disease B eta band rhythms (15-29 Hz) are a commonly observed activity pattern in the brain. They are found with magnetoencephalography (MEG) (1-4), EEG (5, 6), and local field potential (LFP) recordings from neocortex (7-9) and are preserved across species (10). Local beta oscillations and their coordination between regions are implicated in numerous functions, including sensory perception, selective attention, and motor planning and initiation (2,3,6,7,9,(11)(12)(13)(14)(15). Neocortical beta oscillations are disrupted in various neuropathologies, most notably Parkinson's disease (PD), in which treatments that alleviate motor symptoms also reverse the neocortical beta disruption (16,17). Although associations between beta and performance suggest a crucial role in brain function, beta rhythmicity might not be important per se but instead may be an epiphenomenal consequence of other important processes. Discovering how beta emerges at the cellular and network levels is crucial to understanding why beta is such a clear predictor of performance in many domains.A major, unresolved point of debate concerns the locus of beta generation. One prominent view is that beta is generated in basal ganglia and thalamic structures and that neocortical beta is an entrained reflecti...