Immunocytochemistry of enkephalin and serotonin distribution in restricted zones of the rostral trigeminal spinal subnuclei: Comparisons with subnucleus caudalis

Abstract

The spinal trigeminal subnucleus caudalis processes nociceptive input from the head. However, physiological and behavioral studies in monkeys and humans indicate that painful stimuli from the central face and oral cavity also project through trigeminal nuclei rostral to the spinal subnucleus caudalis. Both enkephalin (ENK) and serotonin (5-HT) are present in rostral trigeminal nuclei and these regions receive inputs from the raphe complex. Thus, it appears that elements of pain-modulating circuitry proposed by Basbaum and Fields (Annu. Rev. Neurosci., 7:309-338, 1984) for the spinal and medullary dorsal horn may also exist in this region. In order to begin an exploration of this circuitry, the present study combines the techniques of retrograde transport of HRP from the ventral posteromedial thalamic nucleus (VPM) of the cat's thalamus to label trigeminothalamic relay cells. Secondarily, immunocytochemical techniques are employed to define the distribution patterns of ENK and 5-HT cells and terminals in relationship to both labeled and nonlabeled neurons in each of the subnuclei of the spinal trigeminal nucleus. Trigeminothalamic relay cells were observed in laminae I and II, the magnocellular region, and the interstitial nucleus (IN) of subnucleus caudalis (Vc). ENK was found in axodendritic and axosomatic terminals, together with a population of small fusiform neurons in all these same areas except the magnocellular region. ENK axosomatic contacts innervated approximately 30% of labeled relay cells, chiefly in lamina I and the IN, or small unlabeled neurons in the same area. Serotonin activity occurred principally in lamina I and the IN and was confined almost exclusively to axodendritic terminals. Examination of subnucleus interpolaris (Vi) revealed relay cells distributed throughout the length of the nucleus and increasing in numbers at rostral levels. A rostral extension of the IN was found just ventrolateral to the main body of Vi and contained numerous labeled cells. The distribution of ENK activity was restricted to the ventral part of Vi and the IN and occurred in axodendritic and axosomatic terminals. These latter elements innervated 30-40% of labeled relay cells in Vi, particularly those located in the IN. Cells containing ENK generally resembled the fusiform cells found in Vc and were distributed in ventral Vi and the IN. Some ENK cells were larger, displayed several dendrites, and occurred only in the ventral Vi. Serotonin within Vi and Vc was confined principally to axodendritic terminals.(ABSTRACT TRUNCATED AT 400 WORDS)

Spontaneous Discharge and Peripherally Evoked Orofacial Responses of Trigemino–Thalamic Tract Neurons during Wakefulness and Sleep

“…This was accomplished by combining extracellular recording methodologies with classical antidromic techniques to identify TGT neurons in unanesthetized cats. The basic physiological characteristics of these neurons, i.e., antidromic latency and conduction velocity, and their anatomical location substantiate results obtained for TGT neurons in acute anesthetized cats (Mizuno, 1970;Dubner and Sessle, 1971;Sessle and Greenwood, 1976;Dostrovsky and Hellon, 1978;Burton and Craig, 1979;Hu et al, 1981;Sessle and Hu, 1981;Matsushita et al, 1982;Hyashi et al, 1984;Matthews et al, 1987;Sunada et al, 1990;Ro and Capra, 1994).…”

“…Both electrophysiological (Sessle and Greenwood, 1976;Sessle and Hu, 1981;Azerad et al, 1982;Sunada et al, 1990;Ro and Capra, 1994) and anatomical labeling (Mizuno, 1970;Woda et al, 1977;Burton and Craig, 1979;Matsushita et al, 1982;Shigenaga et al, 1986;Matthews et al, 1987Matthews et al, , 1989) studies performed in acute anesthetized cats have demonstrated that the rostral trigeminal sensory nuclear complex (TSNC) comprising, respectively, the nucleus oralis and the main sensory nucleus, contains a high density of TGT neurons. Recently, we have shown that the tooth pulp-evoked activity of rostral TSNC neurons is suppressed specifically during the behavioral state of active (AS) or REM sleep .…”

Anatomical distribution of serotonin‐containing neurons and axons in the central nervous system of the cat

“…1c, P6-P18) (Matthews et al, 1987(Matthews et al, , 1989. 1c, P6-P18) (Matthews et al, 1987(Matthews et al, , 1989.…”

Brain sites involved in the antinociceptive effect of bradykinin in rats

“…Stimuli originated in the dental pulp reach the trigeminal nucleus, an area that contains excitatory interneurons involved in the jaw‐opening reflex (Hu et al , 1986). Furthermore, the oral and interpolar parts of the spinal trigeminal nucleus receive neural input from brain centers involved in the nociceptive control (Matthews et al , 1984; Sessle, 1987). Microinjection of BK (4 nmol) into the principal trigeminal nucleus induced an antinociceptive effect with a maximum response (IA = 0.59±0.19) 25 min after (Figure 5A).…”