Orthodontic Force Facilitates Cortical Responses to Periodontal Stimulation

Abstract

Somatosensory information derived from the periodontal ligaments plays a critical role in identifying the strength and direction of occlusal force. The orthodontic force needed to move a tooth often causes uncomfortable sensations, including nociception around the tooth, and disturbs somatosensory information processing. However, it has mostly remained unknown whether orthodontic treatment modulates higher brain functions, especially cerebrocortical activity. To address this issue, we first elucidated the cortical region involved in sensory processing from the periodontal ligaments and then examined how experimental tooth movement (ETM) changes neural activity in these cortical regions. We performed in vivo optical imaging to identify the cortical responses evoked by electrical stimulation of the maxillary and mandibular incisor and the first molar periodontal ligaments in the rat. In naïve rats, electrical stimulation of the mandibular periodontal ligaments initially evoked neural excitation in the rostroventral part of the primary somatosensory cortex (S1), the ventrocaudal part of the secondary somatosensory cortex (S2), and the insular oral region (IOR), whereas maxillary periodontal ligaments elicited excitation only in S2/IOR rostrodorsally adjacent to the mandibular periodontal ligament-responding region. In contrast, maximum responses to mandibular and maxillary periodontal stimulation were observed in S1 and S2/IOR, and the 2 responses nearly overlapped. One day after ETM (maxillary molar movement by Waldo's method), the maximum response to stimulation of the maxillary molar periodontal ligament induced larger and broader excitation in S2/IOR, although the initial responses were not affected. Taken together with the histologic findings of IL-1β expression and macrophage infiltration in the periodontal ligament of the ETM models, inflammation induced by ETM may play a role in the facilitation of S2/IOR activity. From the clinical viewpoints, the larger amplitude of cortical excitation may induce higher sensitivity to pain responding to nonnoxious stimuli, and enlargement of the responding area may reflect radiating pain.

Spike Timing Rigidity Is Maintained in Bursting Neurons under Pentobarbital-Induced Anesthetic Conditions

“…Multiple extracellular recordings were performed from the IC, including granular and dysgranular IC ( Figure 1A ), which receive somatosensory inputs from oral structures (Horinuki et al, 2015; Nakamura et al, 2015). We recorded spontaneous neural activity from 58 neurons under both awake and pentobarbital-induced anesthetic conditions.…”

“…The IC processes nociception and is considered to integrate nociception with limbic information (Hanamori et al, 1998; Horinuki et al, 2015; Nakamura et al, 2015), and plays a pivotal role in regulating oral functions and integrating interoceptive states into conscious feelings (Naqvi and Bechara, 2009). Ropivacaine hydrochloride (AstraZeneca, Osaka, Japan), a long-lasting local anesthetic, was applied to the incisions to avoid the production of pain after awaking from anesthesia.…”

Anatomical aspects of corticotrigeminal projections to the medullary dorsal horn

“…Electrical stimulation of dental pulp principally activates the border between S2 and IC caudally adjacent to the middle cerebral artery, named S2/IOR [29][30][31][32][33][34][35]. In contrast to S2/IOR activation, S1 exhibits less activation by dental pulp stimulation, which is also true for electrical stimulation of the periodontal ligament [36,37]. It is worth noting that mechanical stimulation of the periodontal ligament, by pulling the maxillary first molar, induces greater S1 activation than S2/IOR activation [38,39].…”

Opposite effects of mu and delta opioid receptor agonists on excitatory propagation induced in rat somatosensory and insular cortices by dental pulp stimulation

“…Stimulation of the agranular IC, the ventral part of the IC, suppresses nociceptive responses via modulating neural activities of the dorsal raphe nucleus, periaqueductal gray, and parabrachial nucleus [5]. In terms of orofacial nociception, the insular oral region (IOR) and the dorsally adjacent secondary somatosensory cortex (S2), which are located caudal to the middle cerebral artery (MCA) in the rat, respond to electrical stimulation of dental pulps [6,7,8] or periodontal ligaments [9,10]. S2/IOR is likely to encode the strength of nociception because the amplitude of excitation in S2/IOR is dependent on the intensity of molar pulp stimulation [7].…”