The tactile sensitivity of the teeth, and associated periodontium, serves important sensory and motor functions. Microneurographic recordings from human periodontal ligament mechanoreceptor (PDLM) nerves, in response to tooth loading, reveal discharge patterns with sole slowly adapting (SA) II-type characteristics, highlighting the unique role of PDLMs in oral sensory processes. Here we investigate these receptors' properties, psychophysically and with neuroimaging (fMRI), in response to varying frequencies of dynamic (vibrotactile) stimulation. The finding of increased activity in primary (SI) and secondary (SII) somatosensory cortices (SI and SII) at low frequencies of stimulation (20 Hz) as compared with higher frequencies (50 and 100 Hz), shows an increased entrainment of the PDLMs at this lower frequency in line with expected SA II-type response properties. At the highest frequency (100 Hz), no significant activity was found in SI or SII, suggesting this frequency is outside the range of activity of PDLMs. An activation matrix is mapped that includes SI, SII, insular, inferior frontal gyrus, inferior parietal lobe and supplementary motor area as well as middle frontal gyrus and cerebellum. We compared the responses to tooth stimulation with those produced by identical vibrotactile stimulation of the finger. The results strongly suggest that the PDLMs play a significant role in the specification of the forces used to hold and manipulate food between teeth, and in these respects, the masticatory system appears analogous to fine finger-control mechanisms used during precision manipulation of small objects. Because fMRI reveals activations in posterior insular cortex, we also speculate that PDLMs, and SA II-type receptors in general, may be involved in one aspect of the feeling of body ownership.