Periodontal tactile input activates the prefrontal cortex

www.nature.com/scientificreports OPEN Periodontal tactile input activates the prefrontal cortex Nobuaki Higaki, Takaharu Goto & Tetsuo Ichikawa received: 05 April 2016 accepted: 21 October 2016 Published: 11 November 2016 The prefrontal cortex (PFC) plays a role in complex cognitive behavioural planning, decision-making, and social behaviours. However, the effects of sensory integration during motor tasks on PFC activation have not been studied to date. Therefore, we investigated the effect of peripheral sensory information and external information on PFC activation using functional near-infrared spectroscopy (fNIRS). Cerebral blood flow (CBF) was increased around bilateral Brodmann areas 46 and 10 during visual and auditory information integration during an occlusal force (biting) task. After local anesthesia, CBF values were significantly decreased, but occlusal force was similar. In conclusion, the effects of peripheral sensory information from the periodontal ligament and external information have minimal impacts on occlusal force maintenance but are important for PFC activation. The prefrontal cortex (PFC) is located in the anterior region of the cerebral cortex and plays a role in complex cognitive behavioural planning, decision-making, and social behaviors1–3. The contributions of the PFC to cognitive performance and working memory are a mechanism for active information maintenance as well as maintained information processing. A large number of neuroimaging studies have evaluated activation of the PFC using functional magnetic resonance imaging (fMRI) and functional near-infrared spectroscopy (fNIRS) in humans. PFC activation is reported to increase during working memory tasks such as the n-back task and the random number generation task4,5. The PFC can be divided into the dorsolateral prefrontal cortex (DLPFC), the orbitofrontal cortex, frontal pole, and the anterior cingulate cortex (ACC). The DLPFC and ACC are known to be activated in response to incongruent stimuli, consistent with a role in the implementation of cognitive control and performance monitoring6. Botvinick and colleagues reported that the ACC was activated in response to Stroop task stimuli, further relating its function to cognitive control7. Additionally, recent neuroimaging studies in patients with PFC-related dysfunction have informed the clinical significance of the PFC. Schizophrenic patients demonstrate impaired procedural learning as assessed by the Tower of Hanoi test8, and indeed it has been reported that schizophrenia patients show decreased PFC activation during working memory tasks relative to healthy controls9. Mah and colleagues reported that patients with lesions in the PFC show poor insight into their own deficits, and rely primarily on nonverbal cues to make inter personal judgments during the Interpersonal Perception Task10. Moreover, the relationship between decreased activation of the PFC and reductions in communication, social behaviour, affection, self-motivation, and cognitive function has been highlighted in dementia patients11. Kawashima et al. reported that learning tasks such as reading aloud and performing simple arithmetic might be useful for activating the PFC to prevent cognitive impariment12. Activation of the PFC has been also discussed in the context of autokinetic tasks. Many brain regions are associated with autokinesis, such as the primary motor area, the prefrontal area, the supplementary motor area, the basal ganglia, and the cerebellum. Matsumura and colleagues reported that the PFC is more highly activated during the grasping task than the touch task using positron emission tomography (PET)13. Indeed, increased CBF in the PFC has been reported during toe flexion-extension movements14, shoulder flexion-extension movements15, and mouth opening and closing16. Regarding oral autokinesis, Narita and Otsuka reported that the simulated chewing task increases CBF in the PFC17,18. However, these previous studies only compared activation of the PFC between two different tasks, such as the finger relaxing and movement tasks or the foot and finger movement tasks. It is possible that different movement tasks have different degrees of impact on CBF in the PFC. Therefore, a movement task with the elimination of peripheral sensory information should be utilized to evaluate the intrinsic effect of peripheral sensory information on the PFC. However, the relationship between peripheral sensory information and activation of the PFC has not yet been evaluated. Further, there are few reports on the effect of sensory input during a motor task on PFC activation. Department of Oral and Maxillofacial Prosthodontics, Institute of Biomedical Sciences, Tokushima University Graduate School, 3-18-15 Kuramoto, Tokushima 770-8504, Japan. Correspondence and requests for materials should be addressed to T.G. (email: ) Scientific Reports | 6:36893 | DOI: 10.1038/srep36893 1 www.nature.com/scientificreports/ Figure 1. (a) Typical topographical patterns of cerebral blood flow (CBF) in the prefrontal cortex (PFC) before anesthesia. (b) Typical topographical patterns of CBF in the PFC after local anesthesia. (c) Typical topographical patterns of CBF in the PFC after anesthesia in biting in the contralateral side (non-local anesthesia side). (d) Typical topographical patterns of CBF in the PFC after surface anesthesia. Therefore, we studied the PFC by focusing on oral movements and periodontal tactile sensation, which is easy to eliminate during a motor task. The effect of peripheral sensory information and external information on PFC activation was investigated by asking subjects to maintain occlusal force (periodontal tactile input) with the guidance of visual and auditory information. Results Figure 1 shows the typical topographical CBF patterns in the PFC upon task completion. Red and blue indicate CBF increases and decreases, respectively. In the task before local anesthesia, a strong red colour was observed in almost all regions, but a weak blue colour was identified in part of area 10 (Fig. 1a). No red was observed at rest, and blue was observed in areas 10 to 46 in the right hemisphere. After local anesthesia, diffuse red colouring was observed in almost all regions (Fig. 1b). The topographical patterns in the contralateral side (no local anesthesia) during the task after local anesthesia, as well as in the task after only surface anesthesia, were similar to those in the task before local anesthesia (Fig. 1c,d). Both were different from the patterns observed in the ipsilateral side after anesthesia. Figure 2 shows typical temporal patterns of CBF and occlusal force during the 30-second task. Before local anesthesia, CBF patterns in the three experimental tasks (visual information only, auditory information only, no external information) monotonically increased around bilateral areas 46 and 10, and occlusal force was maintained at a constant value. Conversely, CBF at rest wa (...truncated)