Somatotopic direct projections from orofacial areas of primary somatosensory cortex to pons and medulla, especially to trigeminal sensory nuclear complex, in rats

Abstract The primary somatosensory cortex (S1) projects to the thalamus and brainstem somatosensory nuclei and modulates somatosensory information ascending to the S1 itself. However, the projections from the S1 to the brainstem second-order somatosensory neuron pools have not been fully studied. To address this in rats, we first revealed the somatotopic representation of orofacial areas in the S1 by recording cortical surface potentials evoked by stimulation of the lingual, mental, infraorbital, and frontal nerves. We then examined the morphology of descending projections from the electrophysiologically defined orofacial S1 areas to the pons and medulla after injections of an anterograde tracer, biotinylated dextranamine (BDA), into the orofacial S1 areas. BDA-labeled axon terminals were seen mostly in the trigeminal sensory nuclear complex (TSNC) and had a strong contralateral predominance. They also showed a somatotopic arrangement in dorsoventral and superficial-deep directions within almost all rostrocaudal TSNC levels, and in a rostrocaudal direction within the trigeminal caudal subnucleus. In the principal nucleus (Vp) or oral subnucleus (Vo) of TSNC, the BDA-labeled axon terminals showed a somatotopic arrangement closely matched to that of the electrophysiologically defined projection sites of orofacial primary afferents; these projection sites were marked by injections of a retrograde tracer, Fluorogold (FG), into the Vp or Vo. The FG injections labeled a large number of S1 neurons, with a strong contralateral predominance, in a somatotopic manner, which corresponded to that presented in the electrophysiologically defined orofacial S1 areas. The present results suggest that the orofacial S1 projections to somatotopically matched regions of trigeminal second-order somatosensory neuron pools may allow the orofacial S1 to accurately modulate orofacial somatosensory transmission to higher brain centers including the orofacial S1 itself.