Human periodontal mechanoreceptors : functional properties and role in jaw motor control

Periodontal mechanoreceptors signal information about tooth loads to the central nervous system and are considered to be important for the control of oral motor behaviors, like biting and chewing. Surprisingly, very little is known about the functional properties of periodontal mechanoreceptors at posterior teeth. In this thesis, the technique of microneurography was used on humans to record from single nerve fibers in the inferior alveolar nerve responding to forces applied to the teeth. The basic discharge patterns of human periodontal mechanoreceptors of posterior teeth were analyzed. Receptive field properties, directional sensitivity and encoding of force amplitude and rate were studied. Further, to evaluate the strength of the synaptic coupling between periodontal afferents (and other orofacial mechanoreceptive afferents) and jaw muscle motoneurones, the microneurography technique was combined with electromyography recordings. Finally, in behavioral experiments, the importance of periodontal mechanoreceptors in the regulation of force levels used to hold and split morsels between different types of teeth was attested.

The present results indicate that the innervation of the periodontal ligament is weaker for the posterior teeth compared to the anterior teeth. When the posterior teeth were loaded, all periodontal afferents responded with a slowly adapting response, i.e., they all continued to discharge during sustained tooth loads in at least one direction. The teeth were stimulated in six different directions in the horizontal and vertical planes and the afferents typically responded in two to four of the six directions. However, distally along the dental arch, the afferents showed weaker sensitivity in the vertical directions and a bias in disto-lingual direction for the 1st molar. When stimulating teeth adjacent to the receptor bearing tooth (RBT) about half of the afferents responded to loading of one or two more teeth. This is most likely due to transmission of forces to the RBT because of interdental contacts between the teeth. Thus, mechanical coupling between teeth rather than branching of single nerve fibers explains the multiple-tooth receptive fields.

The majority of the afferents of posterior teeth exhibited a marked curved relationship between the steady-state discharge rate and the amplitude of the stimulated force, featuring a pronounced saturation tendency. Compared to afferents from anterior teeth, these afferents were less sensitive at low force levels. The afferents of posterior teeth were also characterized by a decline in the dynamic sensitivity with increasing force. A quantitative model based on this data revealed that these afferents poorly encode the magnitude of stronger chewing forces. However, a minority of the afferents showed a nearly linear stimulus-response relationship and a small decline in dynamic sensitivity with increased tooth load. Thus, this afferent group will continue to reflect the force profile during higher chewing forces. Strong synaptic coupling between single periodontal afferents and motoneurons of the jaw muscles demonstrated the importance of these receptors for a successful execution of oral function, like mastication. This coupling was mainly unilateral except for the central incisor.

The use of periodontal afferent signals in controlling manipulative and power elements of a biting behavior was studied in a simple hold-and-split task using different types of teeth. The forces used to hold the morsel between the teeth increased distally along the dental arch. Importantly, the difference in hold forces for the various teeth could be explained by the different sensitivity characteristics of the periodontal afferents innervating anterior and posterior teeth. Blocking the sensory input from periodontal afferents increased the magnitude and variability of the hold forces for all types of teeth suggesting that periodontal afferent information is important for the fine motor regulation of the jaw when morsels are manipulated and positioned between the teeth to be prepared for chewing.

List of scientific papers

I. Johnsen SE, Trulsson M (2003). Receptive field properties of human periodontal afferents responding to loading of premolar and molar teeth. J Neurophysiol. 89(3): 1478-87
https://pubmed.ncbi.nlm.nih.gov/12626623

II. Johnsen SE, Trulsson M (2005). Encoding of amplitude and rate of tooth loads by human periodontal afferents from premolar and molar teeth. J Neurophysiol. 93(4): 1889-97. Epub 2004 Nov 24
https://pubmed.ncbi.nlm.nih.gov/15563554

III. Turker KS, Johnsen SE, Trulsson M (2005). Evidence for synaptic coupling between orofacial mechanoreceptors and human jaw muscles. [Manuscript]

IV. Johnsen SE, Svensson KG, Trulsson M (2005). Forces applied by anterior and posterior teeth and roles periodontal afferents during hold-and-split tasks in human subjects. [Manuscript]