Research Article: Negative BOLD responses during hand and foot movements: An fMRI study

Date Published: April 19, 2019

Publisher: Public Library of Science

Author(s): Hiroki Nakata, Ryo Domoto, Nobuaki Mizuguchi, Kiwako Sakamoto, Kazuyuki Kanosue, Andreas Mierau.

http://doi.org/10.1371/journal.pone.0215736

Abstract

The present study employed functional magnetic resonance imaging (fMRI) to examine the characteristics of negative blood oxygen level-dependent (Negative BOLD) signals during motor execution. Subjects repeated extension and flexion of one of the following: the right hand, left hand, right ankle, or left ankle. Negative BOLD responses during hand movements were observed in the ipsilateral hemisphere of the hand primary sensorimotor area (SMI), medial frontal gyrus (MeFG), middle frontal gyrus (MFG), and superior frontal gyrus (SFG). Negative BOLD responses during foot movements were also noted in the bilateral hand SMI, MeFG, MFG, SFG, inferior frontal gyrus, middle temporal gyrus, parahippocampal gyrus, anterior cingulate cortex, cingulate gyrus (CG), fusiform gyrus, and precuneus. A conjunction analysis showed that portions of the MeFG and CG involving similar regions to those of the default mode network were commonly deactivated during voluntary movements of the right/left hand or foot. The present results suggest that three mechanisms are involved in the Negative BOLD responses observed during voluntary movements: (1) transcallosal inhibition from the contralateral to ipsilateral hemisphere in the SMI, (2) the deactivated neural network with several brain regions, and (3) the default mode network in the MeFG and CG.

Partial Text

Recent neuroimaging studies using functional magnetic resonance imaging (fMRI) reported not only increases, but also decreases in blood oxygen level-dependent (BOLD) signals during tasks. These decreases are often referred to as ‘Negative BOLD responses’, and several phenomena have been suggested to be involved. The first involves transcallosal inhibition from one hemisphere to the other. BOLD signals generally increase in the primary motor area (MI) of the contralateral hemisphere during the voluntary movement of a limb, but decrease in the MI ipsilateral to the movement [1–8]. The second phenomenon involves the task-related deactivation of associated areas that belong to an irrelevant sensory modality. For example, deactivation of the visual cortex occurs during somatosensory (tactile) discrimination tasks [9–12]. The third involves the “blood steal” phenomenon. When BOLD signals in some parts of the primary visual cortex increase after particular types of visual stimuli, signals in other parts of the visual cortex decrease [13, 14]. This is often explained by the blood steal phenomenon, which occurs due a decrease in blood flow (i.e. Negative response) in regions that are adjacent to activated regions with increased blood flow (i.e. Positive response) and supplied by a common artery. However, if the distance between Negative and Positive BOLD foci is large (e.g., left and right hemispheres, and frontal and occipital cortices), it is difficult to explain the relationship between Negative and Positive BOLD responses by the blood steal phenomenon [15]. The fourth is related to default mode network. This phenomenon comprises task-independent deactivation regions during the baseline or resting state of the brain involving a specific set of mental operations [16–18].

As described in the Introduction section, many studies have demonstrated deactivation in the ipsilateral MI during voluntary hand movements, suggesting transcallosal inhibition from one hemisphere to the other [1–8]. To the best of our knowledge, only one study has reported deactivation in brain regions other than the ipsilateral MI during actively initiated movements [2], and deactivation was observed in the precuneus when subjects performed a right-handed pinch grip. However, since only six right-handed subjects were used in that study, deactivation regions need to be confirmed using a larger number of subjects.

Negative BOLD responses during hand movements were observed not only in the ipsilateral hemisphere of SMI, but also in other brain regions, such as the MeFG, MFG, and SFG. Furthermore, Negative BOLD responses during foot movement were detected in the bilateral hand SMI as well as in the MeFG, SFG, IFG, MTG, PHG, ACC, CG, fusiform gyrus, and precuneus. There were also two common deactivated regions, the MeFG and CG, which were independent of the movements of the upper and lower limbs. These regions closely corresponded to the default mode network, which was previously reported.

 

Source:

http://doi.org/10.1371/journal.pone.0215736

 

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