Reconsideration of the Autonomic Cranial Ganglia: An Immunohistochemical Study of Mid‐Term Human Fetuses

Abstract

The cranial parasympathetic ganglia have been reported to paradoxically contain the sympathetic nerve marker, tyrosine hydroxylase (TH), in addition to neurons expressing parasympathetic markers such as vasoactive intestinal peptide (VIP) and neuronal nitric oxide synthase (nNOS). However, the distribution of these molecules in the cranial ganglia of human fetuses has not yet been examined. Using paraffin sections from 10 mid-term human fetuses (12-15 weeks), we performed immunohistochemistry for TH, VIP, and nNOS in the parasympathetic ciliary, pterygopalatine, otic, and submandibular ganglia, and for comparison, the sensory inferior vagal ganglion. The ciliary and submandibular ganglia contained abundant TH-positive neurons. In the former, TH-positive neurons were much more numerous than nNOS-positive neurons, whereas in the latter, nNOS immunoreactivity was extremely strong. No or a few cells in the pterygopalatine, otic, and inferior vagal ganglia expressed TH. Ciliary TH neurons appeared to compensate for classically described sympathetic fibers arising from the superior cervical ganglion, whereas in the submandibular ganglion, nNOS-positive neurons as well as TH neurons might innervate the lingual artery in addition to the salivary glands. Significant individual variations in the density of all these markers suggested differences in sensitivity to medicine affecting autonomic nerve function. Consequently, in the human cranial autonomic ganglia, it appears that there is no simple dichotomy between sympathetic and parasympathetic function. Anat Rec, 295:141-149, 2012. V V C 2011 Wiley Periodicals, Inc.

Dorsal root ganglion neurons and tyrosine hydroxylase—an intriguing association with implications for sensation and pain

“… (A) Adult TH-expressing DRG neurons have been detected in a number of species, including rat, guinea pig and mouse (—, not determined; * in humans, only embryonic expression has so far been studied [43]). (B) TH-expressing mouse DRG neurons are primarily small and medium-sized.…”

A ganglion cell cluster along the glossopharyngeal nerve near the human palatine tonsil

“…Several reports have documented the paradoxical presence of both sympathetic and parasympathetic nerve markers in the human nervous system, although rather than nNOS, vasoactive intestinal peptide (VIP) has been used as a parasympathetic nerve marker: e.g. VIP-positive neurons in the prevertebral sympathetic ganglia [17]; TH-positive neurons in the ciliary parasympathetic ganglion [8,18], in the submandibular parasympathetic ganglion [18], and in the parasympathetic pelvic ganglia [2,3]. The intrapharyngeal ganglion of the cat near the palatine tonsil carries not only abundant VIP-positive neurons but also a few TH-positive neurons [10].…”

“…TH is a rate-limiting enzyme of catecholamine synthesis in sympathetic ganglion cells, whereas nNOS is a key enzyme in the production of nitric oxide, a molecule that directly regulates vasorelaxation and blood supply, and a well-known marker of parasympathetic neurons. In humans, nNOS reactivity has been investigated particularly in the pelvic nerves [6,7] but previous descriptions for the head region have been limited to the cranial ganglia of the autonomic nervous system [8,9].…”

Significant Differences in Sympathetic Nerve Fiber Density Among the Facial Skin Nerves: A Histologic Study Using Human Cadaveric Specimens

“…Likewise, in the V2 and V3 of cats, Hoffmann and Matthews () reported that sensory fibers are much greater in number than sympathetic fibers in contrast to the median and ulnar nerves. No or few sympathetic nerve fibers seemed to be transferred in the infratemporal and pterygopalatine fossae from artery‐bounded sympathetic nerves as well as from the nearby ganglia although the human pterygopalatine and otic ganglia contain TH‐positive neurons (Kiyokawa et al, ).…”

“…contrast to the median and ulnar nerves. No or few sympathetic nerve fibers seemed to be transferred in the infratemporal and pterygopalatine fossae from arterybounded sympathetic nerves as well as from the nearby ganglia although the human pterygopalatine and otic ganglia contain TH-positive neurons (Kiyokawa et al, 2012). Kashima et al (2013) reported that the basic taste stimuli elicit regional differences in the facial skin blood flow without simultaneous systemic circulatory changes.…”