Alpha-band desynchronization in human parietal area during reach planning

https://doi.org/10.1016/j.clinph.2014.07.026Get rights and content

Highlights

  • Posterior parietal cortex (PPC) uses frequency-specific dynamics in planning visuo-motor goal-directed tasks.

  • Upper alpha band PPC activity codes for preparing goal-directed actions, whereas lower alpha band PPC activity reflects general task demands and attentional processes that are not task-specific.

  • PPC activates earlier in a goal-directed action.

Abstract

Objective

The symptoms with optic ataxia suggest that simple and visually guided hand movements are controlled by 2 different neural substrates. To assess the differential frequency-coded posterior parietal cortex (PPC) role in planning visuo-motor goal-directed tasks, we studied the action specificity of event-related desynchronization (ERD) in this area.

Methods

We investigated cortical activity by electroencephalography, while 16 healthy subjects performed self-paced reaching or wrist extension (control) movements. Time–frequency representations were calculated for each movement during the preparatory period.

Results

ERD dynamics in upper alpha-band indicated that preparing a goal-directed action activates contralateral PPC to the moving hand around 1.2 s before starting the movement, while this activation is later (around 0.7 s) in preparing a not-goal-directed action. The posterior dominant rhythm had peak frequency of lower alpha-band at bilateral parietal.

Conclusions

Posterior parietal cortex encodes goal-directed movement preparation through upper alpha-band activity, whereas general attention is processed via lower alpha-band oscillations.

Significance

Preparing to reach an object engages posterior parietal cortex earlier than a not-goal directed movement.

Introduction

Reaching for an object is a type of complex hand movement performed by humans and primates, and is often called visually guided reaching or praxis. We reach for objects with an incredibly high degree of precision in daily life. Such behavior appears to be effortless, even with unexpected perturbations such as an object relocation (Prablanc and Martin, 1992, Pisella et al., 2000). However, reaching movements require integrated information regarding the object’s position and orientation to guide the hand to the object with accuracy, whereas information regarding the object’s shape and size determines how the fingers move opposite to the thumb to grasp the object. Recent functional imaging studies that used functional MRI or PET in humans have revealed that the posterior parietal cortex (PPC) plays an important role in controlling praxis movements by continuously integrating sensory information regarding the body state and environment (Culham et al., 2006). However, these modern techniques provide temporal resolution that is insufficient for reliable quantitative analysis of activation times.

In humans and primates, motor-related activity has been successfully investigated through electroencephalographic (EEG) oscillatory activity analysis. It is well known that event-related desynchronization (ERD) in the alpha-band (8–13 Hz) starts about 1.5 s before the onset of movement (Pfurtscheller and Berghold, 1989). This activity is presumed to reflect cortical activity related to movement planning (Pfurtscheller and Lopes da Silva, 1999). Experimental data suggest that alpha ERD represents an electrophysiological correlate of activated cortical areas that is related to information processing, selective attention, and motor preparation (Van Winsum et al., 1984, Pfurtscheller, 1992, Dujardin et al., 1993, Dujardin et al., 1995). Furthermore, Pfurtscheller et al. (2000) reported that in a motor task, the upper frequency mu rhythms (10–12 Hz) reflects a more somatotopic spatial ERD pattern than the lower frequency mu rhythms (8–10 Hz). This different behavior between the lower and upper alpha-band components indicates that the lower alpha ERD reflects general task demands and attentional processes that are not task-specific, whereas the upper alpha ERD develops when movement-related information is processed; therefore, it is task-specific (Pfurtscheller et al., 2000). In addition, the posterior dominant rhythm (PDR) is an idling rhythm, indicative of a relative decrease in conscious attention or visual processing (Pfurtscheller and Aranibar, 1977). Approximately 80% of healthy adults had a PDR between 9 and 11 Hz (Kellaway, 1990).

Movement-specific ERD has been recorded not only from scalp electrodes but also subdural electrodes (Toro et al., 1994). However, only a few investigations have used this approach to study more practical and coordinated movements such as reaching, catching, or grasping (Tombini et al., 2009, Van Der Werf et al., 2010, Virji-Babul et al., 2010).

The present study aimed to clarify the involvement of PPC in movement planning and execution by revealing upper alpha-band ERD in parietal area, when reaching for an object (i.e., target- and body-related movements). Therefore, we compared reaching and simple movements to determine whether the underlying neural sources of EEG activity for these movements can be distinguished as independent.

Section snippets

Participants

Subjects were 16 healthy right-handed university students (6 men, 10 women; age, 22–25 years) with normal or corrected-to-normal vision and with no reported history of neurological or psychiatric illnesses. All subjects provided an informed consent for participating in the study. The Ethical Committee of Kyoto University approved the experimental protocol (No. E-929).

Recording conditions

EEG signals from 23 Ag/AgCl surface electrodes placed on the scalp were recorded according to the 10–10 International System. For

Results

Data from a subject was excluded from the statistical analysis because an insufficient number of trials were recorded. In addition, data from another subject including significant artifacts during left wrist extensions was excluded.

Fig. 2A presents grand-average mapped spatially enhanced alpha ERD for reaching and wrist extension. In the grand-averaged ERD, the 12-Hz frequency band revealed the highest power decreases relative to baseline (Fig. 2A). A three-way repeated-measures ANOVA revealed

Discussions

The aim of this study was to determine the temporal characteristics and spatial distribution of brain regions activated during the planning of reaching and wrist extension movements. We identified 3 main differences between these 2 movement conditions in the ERD analysis. The first difference was in the distribution of 12-Hz ERD that revealed a task-specific pattern (Figs. 2A and 3). We estimated the upper alpha-band activity involved in reach planning was located in the parietal area

Conclusions

In conclusion, the present EEG investigation supports the working hypothesis that alpha ERD in the parietal area provides complementary information on brain activity in humans during the preparation and execution of volitional reaching movements. Our main finding was that alpha ERD originating from the parietal area encodes the reaching movement, whereas alpha ERD originating from fronto-central (e.g., suppression of the mu rhythm) and the anterior region of the parietal area encodes wrist

Acknowledgements

This work was supported by Grants-in-Aid for Scientific Research (B) 26282218, 26293209, (C) 26330175 from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (MEXT).

Conflict of interest: The authors declare no competing financial interests.

References (32)

Cited by (14)

  • EEG, MEG and neuromodulatory approaches to explore cognition: Current status and future directions

    2021, Brain and Cognition
    Citation Excerpt :

    Increased alpha synchronisation (or ERS) over the stimuli-ipsilateral hemisphere and alpha desynchronisation (or ERD) in the stimuli-contralateral lobe are observed during attention (Van Moorselaar & Slagter, 2020), WM encoding and maintenance (Van Ede, 2018) in both visual (De Vries et al., 2019; De Vries et al., 2019; De Vries, van Driel, & Olivers, 2017; De Vries, van Driel, Karacaoglu, & Olivers, 2018; Popov et al., 2018; Román-López et al., 2019; Schneider et al., 2019; Van Ede et al., 2019) and auditory (Klatt et al., 2019; Pavlov & Kotchoubey, 2020; Woestmann et al., 2020) modalities. Alpha power decreases, and ERDs are also observed in the sensorimotor cortex during somatosensory and motor planning/execution tasks (Fumuro & Matsuhashi et al., 2015, 2018; Pfurtscheller & Da Silva, 1999). The spatial patterns of synchronisation and desynchronisation may index brain sites that are, respectively, contributing to or uninvolved in information processing.

  • The role of cortical sensorimotor oscillations in action anticipation

    2017, NeuroImage
    Citation Excerpt :

    During the execution of different movement types, low frequency mu (8–10 Hz) shows a widespread movement-type non-specific activity pattern, which was suggested to be indicative of a somatotopically non-specific activation, and related to more general attentional processes (Pfurtscheller et al., 2000). Higher frequency mu (11–13 Hz) on the other hand shows a focused, movement-type specific pattern suggesting activation of somatotopically specific cortical networks (Pfurtscheller et al., 2000) during goal directed movements (Fumuro et al., 2015). Thus far, researchers have only focused on action execution, however on the basis of mirror system principles it would be predicted that these findings should be found in observation tasks.

  • Correlation between cortical and subcortical neural dynamics on multiple time scales in Parkinson's disease

    2015, Neuroscience
    Citation Excerpt :

    Another finding of the present study was the dominant expression of multiscale interactions only for the left STN and with centro-parietal dominance. While the latter finding might suggest an increased involvement of motor and associative cortical regions during task performance (Pfurtscheller and Lopes da Silva, 1999; Palva and Palva, 2007; Fumuro et al., 2015; Weiss et al., in press), the observed hemispheric asymmetry in the expression of multiscale interactions is supported by previous studies suggesting hemispheric asymmetries in the case of resting state neural dynamics (Medvedev, 2014), a left-hemispheric dominance in language processing (Schurz et al., in press; Weiss et al., in press), and worsening of speech and language production for DBS of the left STN (Schulz et al., 2012). Concluding, we hypothesize that multiscale interactions reflect ongoing collective neural dynamics, most likely distributed across cortical–subthalamic–thalamic networks, which are not directly related to motor aspects of momentary task performance.

View all citing articles on Scopus
View full text