skip to main content


Title: Prefrontal theta modulates sensorimotor gamma networks during the reorienting of attention
Abstract

The ability to execute a motor plan involves spatiotemporally precise oscillatory activity in primary motor (M1) regions, in concert with recruitment of “higher order” attentional mechanisms for orienting toward current task goals. While current evidence implicates gamma oscillatory activity in M1 as central to the execution of a movement, far less is known about top‐down attentional modulation of this response. Herein, we utilized magnetoencephalography (MEG) during a Posner attention‐reorienting task to investigate top‐down modulation of M1 gamma responses by frontal attention networks in 63 healthy adult participants. MEG data were evaluated in the time–frequency domain and significant oscillatory responses were imaged using a beamformer. Robust increases in theta activity were found in bilateral inferior frontal gyri (IFG), with significantly stronger responses evident in trials that required attentional reorienting relative to those that did not. Additionally, strong gamma oscillations (60–80 Hz) were detected in M1 during movement execution, with similar responses elicited irrespective of attentional reorienting. Whole‐brain voxel‐wise correlations between validity difference scores (i.e., attention reorienting trials—nonreorienting trials) in frontal theta activity and movement‐locked gamma oscillations revealed a robust relationship in the contralateral sensorimotor cortex, supplementary motor area, and right cerebellum, suggesting modulation of these sensorimotor network gamma responses by attentional reorienting. Importantly, the validity difference effect in this distributed motor network was predictive of overall motor function measured outside the scanner and further, based on a mediation analysis this relationship was fully mediated by the reallocation response in the right IFG. These data are the first to characterize the top‐down modulation of movement‐related gamma responses during attentional reorienting and movement execution.

 
more » « less
NSF-PAR ID:
10457946
Author(s) / Creator(s):
 ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Human Brain Mapping
Volume:
41
Issue:
2
ISSN:
1065-9471
Page Range / eLocation ID:
p. 520-529
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Previous electro‐ or magnetoencephalography (Electro/Magneto EncephaloGraphic; E/MEG) studies using a correlative approach have shown that β (13–30 Hz) oscillations emerging in the primary motor cortex (M1) are implicated in regulating motor response vigor and associated with an anti‐kinetic role, that is, slowness of movement. However, the functional role of M1 β oscillations in regulation of motor responses remains unclear. To address this gap, we combined EEG with rhythmic TMS (rhTMS) delivered to M1 at the β (20 Hz) frequency shortly before subjects performed an isometric ramp‐and‐hold finger force production task at three force levels. rhTMS is a novel approach that can modulate rhythmic patterns of neural activity. β‐rhTMS over M1 induced a modulation of neural oscillations to β frequency in the sensorimotor area and reduced peak force rate during the ramp‐up period relative to sham and catch trials. Interestingly, this rhTMS effect occurred only in the large force production condition. To distinguish whether the effects of rhTMS on EEG and behavior stemmed from phase‐resetting by each magnetic pulse or neural entrainment by the periodicity of rhTMS, we performed a control experiment using arrhythmic TMS (arTMS). arTMS did not induce changes in EEG oscillations nor peak force rate during the rump‐up period. Our results provide novel evidence that β neural oscillations emerging the sensorimotor area influence the regulation of motor response vigor. Furthermore, our findings further demonstrate that rhTMS is a promising tool for tuning neural oscillations to the target frequency. 
    more » « less
  2. Abstract

    Recent experimental results have shown that the detection of cues in behavioral attention tasks relies on transient increases of acetylcholine (ACh) release in frontal cortex and cholinergically driven oscillatory activity in the gamma frequency band (Howe et al. Journal of Neuroscience, 2017, 37, 3215). The cue‐induced gamma rhythmic activity requires stimulation of M1 muscarinic receptors. Using biophysical computational modeling, we show that a network of excitatory (E) and inhibitory (I) neurons that initially displays asynchronous firing can generate transient gamma oscillatory activity in response to simulated brief pulses of ACh. ACh effects are simulated as transient modulation of the conductance of an M‐type K+current which is blocked by activation of muscarinic receptors and has significant effects on neuronal excitability. The ACh‐induced effects on the M current conductance,gKs, change network dynamics to promote the emergence of network gamma rhythmicity through a Pyramidal‐Interneuronal Network Gamma mechanism. Depending on connectivity strengths between and among E and I cells, gamma activity decays with the simulatedgKstransient modulation or is sustained in the network after thegKstransient has completely dissipated. We investigated the sensitivity of the emergent gamma activity to synaptic strengths, external noise and simulated levels ofgKsmodulation. To address recent experimental findings that cholinergic signaling is likely spatially focused and dynamic, we show that localizedgKsmodulation can induce transient changes of cellular excitability in local subnetworks, subsequently causing population‐specific gamma oscillations. These results highlight dynamical mechanisms underlying localization of ACh‐driven responses and suggest that spatially localized, cholinergically induced gamma may contribute to selectivity in the processing of competing external stimuli, as occurs in attentional tasks.

     
    more » « less
  3. Abstract

    Multiple sclerosis (MS) is a demyelinating disease that results in a broad array of symptoms, including impaired motor performance. How such demyelination of fibers affects the inherent neurophysiological activity in motor circuits, however, remains largely unknown. Potentially, the movement errors associated with MS may be due to imperfections in the internal model used to make predictions of the motor output that will meet the task demands. Prior magnetoencephalographic (MEG) and electroencephalographic brain imaging experiments have established that the beta (15‐30 Hz) oscillatory activity in the sensorimotor cortices is related to the control of movement. Specifically, it has been suggested that the strength of the post‐movement beta rebound may indicate the certainty of the internal model. In this study, we used MEG to evaluate the neural oscillatory activity in the sensorimotor cortices of individuals with MS and healthy individuals during a goal‐directed isometric knee force task. Our results showed no difference between the individuals with MS and healthy individuals in the beta activity during the planning and execution stages of movement. However, we did find that individuals with MS exhibited a weaker post‐movement beta rebound in the pre/postcentral gyri relative to healthy controls. Additionally, we found that the behavioral performance of individuals with MS was aberrant, and related to the strength of the post‐movement beta rebound. These results suggest that the internal model may be faulty in individuals with MS.Hum Brain Mapp 38:4009–4018, 2017. ©2017 Wiley Periodicals, Inc.

     
    more » « less
  4. Key points

    Visual attention involves discrete multispectral oscillatory responses in visual and ‘higher‐order’ prefrontal cortices.

    Prefrontal cortex laterality effects during visual selective attention are poorly characterized.

    High‐definition transcranial direct current stimulation dynamically modulated right‐lateralized fronto‐visual theta oscillations compared to those observed in left fronto‐visual pathways.

    Increased connectivity in right fronto‐visual networks after stimulation of the left dorsolateral prefrontal cortex resulted in faster task performance in the context of distractors.

    Our findings show clear laterality effects in theta oscillatory activity along prefrontal–visual cortical pathways during visual selective attention.

    Abstract

    Studies of visual attention have implicated oscillatory activity in the recognition, protection and temporal organization of attended representations in visual cortices. These studies have also shown that higher‐order regions such as the prefrontal cortex are critical to attentional processing, but far less is understood regarding prefrontal laterality differences in attention processing. To examine this, we selectively applied high‐definition transcranial direct current stimulation (HD‐tDCS) to the left or right dorsolateral prefrontal cortex (DLPFC). We predicted that HD‐tDCS of the leftversusright prefrontal cortex would differentially modulate performance on a visual selective attention task, and alter the underlying oscillatory network dynamics. Our randomized crossover design included 27 healthy adults that underwent three separate sessions of HD‐tDCS (sham, left DLPFC and right DLPFC) for 20 min. Following stimulation, participants completed an attention protocol during magnetoencephalography. The resulting oscillatory dynamics were imaged using beamforming, and peak task‐related neural activity was subjected to dynamic functional connectivity analyses to evaluate the impact of stimulation site (i.e. left and right DLPFC) on neural interactions. Our results indicated that HD‐tDCS over the left DLPFC differentially modulated right fronto‐visual functional connectivity within the theta band compared to HD‐tDCS of the right DLPFC and further, specifically modulated the oscillatory response for detecting targets among an array of distractors. Importantly, these findings provide network‐specific insight into the complex oscillatory mechanisms serving visual selective attention.

     
    more » « less
  5. Abstract

    Increasing spatial working memory (SWM) load is generally associated with declines in behavioral performance, but the neural correlates of load‐related behavioral effects remain poorly understood. Herein, we examine the alterations in oscillatory activity that accompany such performance changes in 22 healthy adults who performed a two‐ and four‐load SWM task during magnetoencephalography (MEG). All MEG data were transformed into the time‐frequency domain and significant oscillatory responses were imaged separately per load using a beamformer. Whole‐brain correlation maps were computed using the load‐related beamformer difference images and load‐related accuracy effects on the SWM task. The results indicated that load‐related differences in left inferior frontal alpha activity during encoding and maintenance were negatively correlated with load‐related accuracy differences on the SWM task. That is, individuals who had more substantial decreases in prefrontal alpha during high‐relative to low‐load SWM trials tended to have smaller performance decrements on the high‐load condition (i.e., they performed more accurately). The same pattern of neurobehavioral correlations was observed during the maintenance period for right superior temporal alpha activity and right superior parietal beta activity. Importantly, this is the first study to employ a voxel‐wise whole‐brain approach to significantly link load‐related oscillatory differences and load‐related SWM performance differences.

     
    more » « less