Long‐term neuroplasticity of the face primary motor cortex and adjacent somatosensory cortex induced by tooth loss can be reversed following dental implant replacement in rats

Abstract

Tooth loss is common, and exploring the neuroplastic capacity of the face primary motor cortex (face-M1) and adjacent primary somatosensory cortex (face-S1) is crucial for understanding how subjects adapt to tooth loss and their prosthetic replacement. The aim was to test if functional reorganization of jaw and tongue motor representations in the rat face-M1 and face-S1 occurs following tooth extraction, and if subsequent dental implant placement can reverse this neuroplasticity. Rats (n = 22) had the right maxillary molar teeth extracted under local and general anesthesia. One month later, seven rats had dental implant placement into healed extraction sites. Naive rats (n = 8) received no surgical treatment. Intracortical microstimulation (ICMS) and recording of evoked jaw and tongue electromyographic responses were used to define jaw and tongue motor representations at 1 month (n = 8) or 2 months (n = 7) postextraction, 1 month postimplant placement, and at 1-2 months in naive rats. There were no significant differences across study groups in the onset latencies of the ICMS-evoked responses (P > 0.05), but in comparison with naive rats, tooth extraction caused a significant (P < 0.05) and sustained (1-2 months) decreased number of ICMS-defined jaw and tongue sites within face-M1 and -S1, and increased thresholds of ICMS-evoked responses in these sites. Furthermore, dental implant placement reversed the extraction-induced changes in face-S1, and in face-M1 the number of jaw sites even increased as compared to naive rats. These novel findings suggest that face-M1 and adjacent face-S1 may play a role in adaptive mechanisms related to tooth loss and their replacement with dental implants.

Widespread Volumetric Brain Changes following Tooth Loss in Female Mice

“…The shrinkage of M1 and S1 is consistent with previous findings of decreased jaw and tongue motor representations and decreased excitability of orofacial M1 and S1 following molar tooth extraction in rodents (Avivi-Arber et al, 2015; Hayashi et al, 2015). Such changes may reflect the documented adaptive or maladaptative processes induced by the altered somatosensory inputs as a result of the missing teeth, injury to gingival, periodontal and pulpal nerves, and/or by compensatory sensorimotor functions caused by the loss of three major food-grinding dental elements (for review see Avivi-Arber et al, 2011; Sessle et al, 2013).…”

“…Consistent with our previously documented electro-physiological and immunohistochemical findings in rats and mice, demonstrating that changes in pain behavior and neuronal responses in the orofacial primary sensorimotor cortex are apparent on days 7–28 following orofacial injury (Zhang S. H. et al, 2006; Avivi-Arber et al, 2010a, 2015; Mashregi et al, 2011; Soleimannejad et al, 2012; Varathan et al, 2014; Hayashi et al, 2015), mice in the present study were killed humanely 21 days postoperatively. All mice were fixation-perfused transcardially and the brains were imaged as described below.…”

“…Changes in the trigeminal brainstem sensory nuclei, thalamus, S1, M1 as well as in other higher order brain regions were documented by us previously (for review see Avivi-Arber et al, 2011; Sessle et al, 2013). For example, we have shown in rodents and humans that changes in somatosensory inputs or altered motor functions induced by intraoral manipulations, including tooth extraction, can result in short-term (days) and long-term (months) functional neuroplasticity in the orofacial S1 and M1 (Adachi et al, 2007; Avivi-Arber et al, 2010a, 2015; Awamleh et al, 2015; Pun et al, 2016). Tooth loss results in decreased motor representation of jaw and tongue muscles and decreased orofacial M1 excitability (Avivi-Arber et al, 2015).…”

“…The mouth was kept open by pulling down the 2 mandibular incisors with a rubber band. In the Extraction group the 3 right maxillary molar teeth were luxated (Avivi-Arber et al, 2010b, 2015). Sham mice had the same general anesthesia and mouth opening but no actual tooth extraction.…”

“…We and others have already shown that tooth extraction in rodents can also induce functional and structural changes in both glial and neuronal cells within brain regions involved in processing orofacial sensory and motor functions as well as cognitive and emotional behaviors (Avivi-Arber et al, 2014, 2015; Varathan et al, 2014; Chen et al, 2015; Watase et al, 2016). High resolution sMRI in rodents can provide an excellent readout of anatomical brain changes in mice following nerve injury, housing in an enriched environment, or maze training and such changes are also associated with cellular and molecular changes (Seminowicz et al, 2009; Lerch et al, 2011b; Cahill et al, 2015; Scholz et al, 2015a).…”