Elsevier

Behavioural Brain Research

Volume 396, 1 January 2021, 112865
Behavioural Brain Research

Cerebral hemodynamics predicts the cortical area and coding scheme in the human brain for force generation by wrist muscles

https://doi.org/10.1016/j.bbr.2020.112865Get rights and content

Highlights

  • Force production by muscle contraction is a basis underlying all movements in our life.

  • fNIRS technique is used to identify the cortical area and activity related to low-level motor control in the human brain.

  • The wrist area dorsal to the finger region is highly active over the primary sensorimotor cortex for isometric force production by wrist muscles.

  • Both amplitude and temporal parameters of oxygenated hemodynamic signals can predict static wrist muscle force over a full physiological range.

Abstract

The goal of this study is to identify the cortical area maximally active over the primary sensorimotor cortex (SM1) and characterize the cortical encoding for force production by wrist muscles in the human brain. The technique of functional near-infrared spectroscopy (fNIRS) was used to continuously monitor the changes in hemoglobin concentrations from the left hemisphere during isometric contractions of wrist flexion muscles over a broad range of load forces (0 ∼ 8 kgf) on the right hand. As previously shown in primate studies, this action produced hemodynamic activity predominantly in the wrist area localized dorsally to the finger region over SM1 and the hemodynamic response was systematically related to the level of load intensity. The coding scheme for force production in terms of hemodynamic signals was characterized defining eight trajectory parameters (four for amplitude coding and four for temporal coding) and analyzed for the area maximally activated over SM1. The trajectory parameter representing the oxygenated hemoglobin concentration change at the end of motor task (amplitude coding) and the timing of maximum change in oxygenated hemoglobin concentration (temporal coding) was most strongly correlated with the load variation in a superliner manner. All these results indicate the applicability of fNIRS to monitor and decode cortical activity that is correlated with low-level motor control such as isometric muscle contractions. This study may provide not only insights into cortical neural control of muscle force but also predictors of muscle force in clinical diagnostics and neural interfaces for the human brain.

Introduction

The ability of the motor system to generate and control muscle force is the basis of all movements performed in daily life. The precentral gyrus (also called the primary motor cortex or M1) is well known as a cortical area of the brain dedicated to producing a wide range of force, from lifting a light sheet of paper (< 1 kgf) to lifting a heavy weight (> 100 kgf) [1,2]. A group of motor cortical neurons has been reported to directly contact spinal motoneurons innervating muscle fibers and precisely control low-level motor behaviors such as flexion or extension of a joint under various loading conditions [[3], [4], [5]]. Thus, understanding the spatiotemporal characteristics of cortical activation for low-level motor control would be a crucial step not only for insights into neural correlates of complex movements but also for the clinical diagnosis and treatment of neurological diseases that induce movement disorders.

The activity pattern of cortical neurons for low-level motor control has been investigated by measuring electrical signals directly from individual neurons in the brains of alert primates [4,6]. These studies using microelectrodes have shown the correlation between neuronal activity and force production by muscles underlying wrist flexion and extension [4] or finger gripping [7] over a low force range. However, invasive approaches may not be applicable to simultaneous measurement over a broad cortical area during motor behavior in humans. Regarding the spatial distribution of cortical activation for low-level motor control, functional magnetic resonance imaging (fMRI) has been applied in humans, showing that the sensorimotor cortex could be involved in the production of finger force under a small, fixed loading force [8]. However, the utility of noninvasive fMRI techniques is restricted by constraints on body movements [9] and low temporal resolution (> a few seconds) [10]. Thus, both invasive electrophysiological and fMRI approaches may be ineffective for spatiotemporal examination of human cortical activity during low-level motor behavior under task settings involving a wide range of force production by various limb muscles.

Over the past few decades, functional near-infrared spectroscopy (fNIRS) has been extensively used as a noninvasive approach for basic and clinical studies of human brain function, mainly due to its tolerance for motion artifacts and the portability of the equipment along with the capacity for low-cost, quiet, safe and continuous measurement with relatively high spatial (10−30 mm) and temporal (up to 100 ms) resolution [[11], [12], [13]]. Using fNIRS, the spatial and temporal aspects of cortical activation have been assessed by measuring the changes in the concentrations of oxygenated and deoxygenated hemoglobin resulting from physiological reactions through neurometabolic [[14], [15], [16]] and neurovascular coupling [[17], [18], [19]] during motor tasks. The ability of fNIRS methodology to identify spatial distributions and temporal patterns of cortical activation [[20], [21], [22], [23], [24], [25], [26], [27]] and functional interactions between active cortical areas during motor task [[28], [29], [30]] has been validated in comparison with conventional noninvasive imaging modalities such as fMRI, magnetoencephalography (MEG) or electroencephalography (EEG).

Most previous studies on brain function using fNIRS techniques have focused on cognitive [31] or high-level motor tasks ranging from finger tapping to dancing [32,33]. A few researches have investigated cortical function related to low-level control of muscle force under the fNIRS system. The previous studies have primarily investigated the functional relationship between degree of cortical activation and force of finger flexion over a limited range (< 50 % of maximal voluntary force) [34,35]. Recently the cortical area and activities associated with wrist movement have been demonstrated in a passive mode using a hand robot [36,37]. Yet, little research has been conducted on cortical area and encoding for voluntary control of wrist muscle contractions at high force levels (> 50 % of maximal voluntary force) in humans.

Here, we aimed at identifying the cortical area maximally active over the primary sensorimotor cortex for isometric force production by wrist muscles and the hemodynamic parameters strongly correlated with isometric force output of wrist muscles over a full physiological range. In this study, it was hypothesized that the maximal hemodynamic response is localized over the cortical area for control of wrist movement in the primary sensorimotor cortex and that the trajectory pattern of hemodynamic signal reflects the force coding schemes observed from corticospinal neurons in primates. The results from this study would be useful not only for neurological diagnosis and treatment assessment of movement disorders but also for brain-machine interfaces for therapeutic purposes.

Section snippets

Preparations

The present study was approved by the Ethics Committee of DGIST (DGIST_180202_HR-001−01) and carried out in accordance with the Declaration of Helsinki. Written informed consent was obtained from all subjects prior to participation. Sixteen healthy male subjects without any history of neurological or psychiatric diseases were recruited for the experiment. Female subjects were not included due to gender differences in physiological properties of cerebral blood flow [38] and skeletal muscles [39

Hemodynamic responses to motor stimulation

The changes in hemoglobin concentration were measured from the left hemisphere while the subjects held various loads on the right hand under isometric conditions. Fig. 2 shows representative responses of oxygenated hemoglobin concentration (△Hboxy, solid lines) to motor stimulation for three load magnitudes (0, 4, and 8 kgf). The maximum change in △Hboxy was assessed for all channels (see Fig. 1D for anatomical locations of individual channels). We found that the cortical area at channel 17 was

Discussion

We demonstrated the possibility that the activity of human cortical areas associated with low-level control of muscle force could be monitored and decoded using a fNIRS approach. As previously shown in primates, the cortical area corresponding to the wrist in the primary sensorimotor cortex (SM1) was the most activated during isometric contractions of wrist flexion muscles. For different levels of load intensity, both the amplitude and peak timing of the oxygenated hemodynamic response

Conclusions

fNIRS technique allows the identification and monitoring of cortical areas and activities for low-level force control of wrist muscles in humans. The wrist area localized dorsally to the finger region in the primary sensorimotor cortex is maximally active during voluntary contractions of wrist muscles over a full physiological range. Over this cortical area, the amplitude of oxygenated hemoglobin concentration change at the task end and the peak timing of oxygenated hemoglobin concentration

Funding

This work was supported by the DGIST R&D Program of the Ministry of Science and ICT, Republic of Korea (18-BT-01, 19-BT-01 and 20-BT-06).

Declaration of Competing Interest

The authors report no declarations of interest.

Acknowledgments

The author thanks Donghyun Kim, Hein Ju, Youngchang Ju, Minjung Kim and Seunghui Cha for their help in bed development, experiment setting and data collection. In addition, the author would like to thank the anonymous reviewers for their constructive and valuable comments on the manuscript.

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