Clinical Characteristics and Lesions Responsible for Swallowing Hesitation After Acute Cerebral Infarction

Nine of the ten patients with swallowing hesitation had a left hemisphere lesion. Interestingly, a few patients with suspicion of dysphagia in our study had a lesion in the left or right capsule or corona radiata. Deglutition and articulatory movements share a common anatomical structure and neurological basis. Some studies demonstrated that dysarthria after a single acute cerebral infarction in the area of the internal capsule or corona radiata is caused significantly and more frequently by a left-side lesion [12, 13]. The corticobulbar tract consists of two groups of fibers, crossing fibers that affect contralateral nuclei and uncrossing fibers that affect ipsilateral nuclei. In other words, nuclei of the medulla are controlled bilaterally by corticobulbar tracts. Therefore, a lesion of a unilateral corticobulbar tract does not ordinarily cause dysphagia. Further, the ratio of the two types of fibers varies among individuals [14]. When a patient has more crossing fibers and fewer uncrossing fibers bilaterally, a unilateral lesion may result in dysphagia. However, the entire picture of the human innate innervation and re-innervation has not been sufficiently revealed. The fact that hesitation does not originate in the motor cortex cannot be denied. Anyway, in this study, a lesion of the internal capsule or corona radiata seemed to have no relationship with swallowing hesitation. Further accumulation of cases and careful longitudinal studies are needed to clarify the relationship between corticobulbar tract and swallowing hesitation.

Four of the five patients with the rippling swallowing hesitation pattern had a lesion in the left primary motor cortex. Moreover, Patient 1 (Case 1) and four who presented rippling tongue movements on VF had a lesion only in the primary motor cortex. The rippling tongue movement appears to be a repetition of trial and error in deglutition. Although the actual motor functions of muscles involved in deglutition are intact, a lack of rhythmical and disciplined coordination of them results in hesitation. The lesion in the primary motor cortex may induce buccofacial apraxia and limb kinetic apraxia as well. Because deglutition contains voluntary and involuntary parts, there is a controversy regarding the application of word “apraxia” for swallowing dysfunction. Notwithstanding, the rippling pattern of swallowing hesitation seems to assume the characteristics of apraxia. Intriguingly, Patient 4 showed the rippling-type swallowing hesitation with a lesion in right primary motor cortex, while Patients 12 and 14, both with lesions including the right primary motor cortex, demonstrated no swallowing hesitation. Thus, the hemisphere dominancy of deglutition might vary among individuals.

On the other hand, the patients with swallowing hesitation characterized by a period of stasis in this study tended to have broad lesions in the left hemisphere. In addition to the primary motor cortex, the orbitofrontal cortex, middle frontal gyrus, inferior frontal gyrus, and insula are entangled at high rates in our patients. For example, Patient 8 (Case 2) showed the typical stasis type of swallowing hesitation due to a broad lesion of the left hemisphere. Lesions in the frontal lobe due to occlusion of the internal carotid artery often become diffuse. In that context, it is noteworthy that Patient 17 (Case 3) with a large part of middle frontal gyrus spared did not show swallowing hesitation, in spite of multiple lesions in the orbitofrontal cortex, inferior frontal gyri, and insula selectively. This indicates us that the lesion of the middle frontal gyrus is important for the establishment of swallowing hesitation, especially the stasis pattern.

The insula, especially its anterior part, receives sensory stimulants in the oral cavity input from nucleus tractus solitarius via the ventroposterior medial nucleus of the thalamus [15]. Further, the anterior part of the insula connects to the primary motor cortex. A lesion of the insula would correlate somewhat with swallowing dysfunction [15] like that seen in this study. The importance of the insula in swallowing is recognized through previous studies, such as a study using functional MRI that demonstrated statistically significant activation in the insula during an oral stereognosis test [16].

Although little is known about the relationship between the middle frontal gyrus and deglutition, some researchers have pointed out the importance of the prefrontal cortex, thought to be involved in higher cognition and containing a large part of middle frontal gyrus. The anterior half of the middle frontal gyrus is redefined as the dorsolateral prefrontal cortex (DLPFC) from a functional perspective and investigated for clinical significance. The DLPFC is not only concerned with self-awareness and attentional control but also involved in executive control of working memory. The prefrontal cortex as a frontal association area is also expected to integrate perceived sensory signals with motor commands [17]. An interplay between the insula as a sensory center, primary motor cortex as a motor center, and middle frontal gyrus as an association area of these is essential for proper deglutition. Of course, the medullary central pattern generator (CPG) also plays an important role in the process of voluntary swallowing, such as adjusting the perception of pieces of food by the sensory input coming from the oral cavity without linkage to cortical levels [18]. We speculated on the neural circuit involved in swallowing (Fig. 2).

As mentioned in the previous three case reports, our patients also had good prognosis for swallowing hesitation. Barer reported that nearly 30 % of 357 patients with a unilateral cerebral lesion were initially found to have difficulty swallowing, but most of their symptoms resolved [6]. When we encounter swallowing hesitation during acute management, we should carefully assess the improvement over time. As mentioned above, nuclei of the medulla receive innervation by the bilateral corticobulbar tracts. Therefore, swallowing hesitation caused by a unilateral lesion may often be improved by enhancement and reorganization of the contralateral innervation [19].

This study had several limitations. First, the results of this research have limited effectiveness because of the small number of cases. To determine the association between swallowing hesitation and the responsible lesion with sufficient statistical power, more patients should be studied. Second, the period from onset to VF of some patients was more than 4 weeks, mainly due to their poor general condition in the acute stage. Ideally, we ought to conduct VF within 2 weeks of onset. In order to obtain further information about swallowing hesitation, we should construct a strict protocol for longitudinal follow-up study in liaison with the sub-acute rehabilitation hospital. Third, because this was a retrospective study, we could not compare the results to those of normal age-matched controls. We are organizing a prospective age-matched control study to obtain firm evidence of swallowing hesitation. Fourth, we did not examine the role of oral sensation in swallowing. Because sensory stimulation inside the oral cavity is one of the important triggers for swallowing, it is important to evaluate the oral sensation of patients with dysphagia. We will consider the oral sensation basis of swallowing hesitation, including trigeminal nerve and brainstem, in the future study. In addition, we will evaluate tongue movement qualitatively for detailed clarification of this pathophysiology. In the future, the degree of hesitation also should be evaluated in detail. Finally, we did not perform statistical analysis of the lesion causing swallowing hesitation. Although we attempted to conduct a multivariate analysis, the small number of cases precluded a statistically meaningful result. We recognize the necessity for continuing accumulation of cases.