Measurement of cerebral blood volume dynamics during volitional swallowing using functional near-infrared spectroscopy: An exploratory study

Highlights

• We examined cerebral blood volume dynamics during volitional swallowing.

• We used a 52-channel functional near-infrared spectroscopy system.

• Increased oxy–Hb was found in the bilateral sensorimotor cortex.

• Increased oxy–Hb was found in the temporal gyrus.

Abstract

The aim of this study was to examine cerebral blood volume dynamics during volitional swallowing using multi-channel functional near-infrared spectroscopy (fNIRS) to understand the basic cortical activation patterns. Fifteen volunteers (age, 26.5 ± 1.3 years, mean ± SD) performed volitional swallowing of a 5-ml bolus of water as a task. A 52-channel fNIRS system was used for measuring oxy–Hb levels. We determined the oxy–Hb concentration changes in each channel by calculating the differences between rest and task oxy–Hb levels. Differences in rest and task data were assessed using a paired-t test (p < 0.05). A significant increase in oxy–Hb was found in 21 channels. The cortical regions that exhibited increased oxy–Hb concentration included the bilateral precentral gyrus, postcentral gyrus, inferior frontal gyrus, superior temporal gyrus, middle temporal gyrus, and supramarginal gyrus. These data provide the first description of cortical activation patterns during volitional swallowing using fNIRS, which will be useful for the evaluation of dysphasia and the effects of the rehabilitation.

Introduction

The act of eating and swallowing is essential for obtaining nutrition, as well as for enjoyment (e.g., the taste, smell, flavor, and texture of foods) and communication while eating. Difficulties in swallowing, termed dysphagia, can occur in a variety of diseases, and increases the risk of aspiration, asphyxiation, pneumonia, nutritional disorders, and dehydration, as well as impacts on patient quality of life.

Swallowing is a reflexive behavior that involves a timely coordinated, bilateral sequence of activation and inhibition of a large number of deglutition related muscles; thus, enabling the transport of a bolus from the oral cavity through the pharynx and esophagus to the stomach while concomitantly protecting the airway [20], [25]. This highly complex, automated motor activity is principally regulated by a central pattern generator (CPG) in the brainstem [19], [25]. However, the initiation of swallowing is partly under voluntary control that requires activity of the cerebral cortex [19]. The cerebral cortex is also considered to connect to the brainstem CPG in coordinated smooth and safe swallowing [1]. Given that cortical dysfunction has been reported to result in swallowing impairment [5], the cerebral cortex plays a crucial role in the initiation and regulation of swallowing. Thus, assessment of cortical activation during swallowing is important to further understand the neural control of swallowing.

Neuroimaging studies using functional magnetic resonance imaging (fMRI) [6], [12], [16], [17], positron emission tomography (PET) [7], and magneto encephalography (MEG) [4] have previously shown that swallowing recruits multiple cerebral regions. Nevertheless, the exact cortical neuroanatomy of swallowing remains unclear. Functional near-infrared spectroscopy (fNIRS) is a recently developed non-invasive neuroimaging technique [14], [31] that measures the concentration changes of oxyhemoglobin (oxy–Hb) and deoxyhemoglobin (doxy–Hb) in the cerebral cortex associated with neural activity [10]. Although fNIRS offers low spatial resolution compared with fMRI or PET, it has a high temporal resolution of 0.1 s [11]. Further, near-infrared light is non-invasive and safe, which enables repeated measurements in an individual [15]. Another advantage of fNIRS is that the apparatus is extremely compact, easily portable, and does not require a special recording room. Further, fNIRS is relatively tolerant of body movements and has no restriction of subject position and location. For example, subjects do not need to be placed in a narrow gantry in a supine position like fMRI or PET, and are examined under more natural conditions throughout the experiment, giving more freedom in task design [21]. Therefore, the application of fNIRS in rehabilitation studies that require motor performance is becoming of increasing interest [29].

To our knowledge, there are no previous reports that have used fNIRS to examine cortical activation while swallowing, and the exact region of the cerebral cortex that is activated during swallowing in a sitting posture is unknown. Thus, in the present study we examined cerebral blood volume dynamics during volitional swallowing using multi-channel fNIRS, and identified the specific regions of the cerebral cortex that exhibited activation.