Invited Review

Histol Histopathol (1998) 13: 1163-1177 Histology and 001: 10.14670/HH-13.1163 Histopathology http://www.hh.um.es From Cell Biology to Tissue Engineering Invited Review Distribution of central catecholaminergic neurons: a comparison between ungulates, humans and other species Y. Tillet1 and K. Kitahama2 1 Laboratory of Sexual Neuroendocrinology, Nouzilly, France and 2Department of Experimental Medicine, School of Medicine, Claude Bernard University, Lyon, France Summary. In ungulates and primates, the distri bution of Introduction central catecho la mine rg ic ne urons identified us in g antibodies raised against catecho lamine synthesizing T he m o noamine rg ic ne uro ns ha ve bee n firs t enzymes and catecholamines themselves, shows many described in rodents by the histoflu orescence method d iffere nces if com pared to rats. Catecho la mine rg ic (Dahlstrom and Fuxe, 1964, 1965; Fuxe, 1965a,b) and neuro ns are more loosely clus tered in ung ul ates and numerous studies have been conducted in these animals. primates tha n in rat. In the medulla o blo ngata, the Investigati o ns in prima tes, pa rtic ul arl y in humans, densit y of noradrenergic/adrenergic neurons is lower in started a few years later (Nobin and Bjorklund, 1973), ungul ates than in other species and, part icularl y in sheep, mainl y for applied medical research considerati on. Only the adrene rg ic g roup C I is no t observed . The no r little attention has been devoted to the other species like adrenergic neuro ns of the locus coeruleus are present in farm animals . Compa ri son of dis tribution of mono a la rger a rea in ung ula tes tha n in ro de nts. In the amine-containing neuro ns between rats and humans hypothalamus, the density of dopamine neurons is lower indicates no tewo rth y species differences in the fine in ungulates and primates than in rodents. In the rostral organization of these neurons. Therefore, it is hazardous hypothalamus of ungul ates, the dorsal part of the group to use information fr om one species to another, and an A l 4 is missing, a nd these s pecies present o nl y the acute kno wl edge of these ne uro na l syste ms seems ve ntral part of the group A 15. In primates the group A 15 indispensable fo r each studied species. extends into the supraoptic and paraventricular nucle i Monoamines are criticall y involved in many neuro which have large tyrosine hydroxylase-immunoreactive endocrine regul ations (reproducti on, growth, lactati on, (TH-IR) ne uro ns no t observed in o the r species. In stress ... ) and autonomic functions, as largely described in addition, in all studied species, not all cells expressing rodents and sometimes in humans (Weiner and Ganong, ca techo lamine sy nthesiz ing e nzy mes a lso e xpress 1978; Tuomisto and Mannisto, 1985; Loewy and Spier, catecholamines, as found in some TH-IR neurons in the 1990). These neuroendocrine and autonomic regulations arcuate nucleus, thereby demonstrating the necessity of a re now s tudied in o the r s pecies s uc h as pigs a nd using di ffe rent markers to ascertain the tru e catechol ruminants w hich constitute an altern ati ve experiment al aminergic nature of labeled neurons. These anatomical mode l to rodents. In additio n, fro m an agric ultural diffe re nces between s pecies s how the difficulty in perspecti ve, there is increasin g interest to understand extrapolating the distribution of catecholamine neurons regul a ti o ns that a ffe ct num e ro us f unc ti o ns a nd f ro m o ne s pec ies to a no th e r a nd m ay be re lated behav ioral patterns in domestic animals. to ad a pta tive physio logical diffe re nces be tween In sheep, a seasonal breede r, dopamine and nor mammals. adrenaline are in volved in the seasonal contro l o f LH secreti on (Thiery et aI. , 1995). In all fa rm animals as Key words: Catecho lamine, Central nervous system, well as in rodents, catecholamines are in volved in the Domesti c mammals, Primates physiological response to stress w hich could decrease animal production (Dantzer et aI. , 1983; Signoret, 1983; Da ntze r, 1986). In pigs a nd rumina nts a uto no mic innervati on of the digesti ve tract pl ays an important role Offprint requests to: Dr. Yves Tillet, Laboratoire de Neuroendocrinologie in the control of digesti on. Sexuell e, INRA-PRMD, 37380 Nouzilly, France. e-mail: tillet@ The pig is used as an experimental model for human tours.inra.fr cardiovascul a r, respira to ry a nd gastro intestina l 1164 Catecholaminergic neurons in mammals physiology (Tumbleson, 1986). In the field of intra it possible to divide them into 2 subgroups: Al/A2 cerebral grafting, neurons of the pig ventral mesence noradrenergic and Cl/C2 adrenergic cell groups. The phalon have been used to correct motor asymmetry in former is composed of caudally situated TH- and DBH the rat model of Parkinson disease (Huffaker et aI., ir cells and is considered to be noradrenergic, and the 1989). In addition, domestic animals could present latter consists of rostrally situated ones which are also neuronal disorders suitable for studying neuro immunoreactive for PNMT and considered to be degenerative processes: sheep scrapy and bovine adrenergic (Hokfelt et aI., 1974, 1984a; Howe et aI., spongiform encephalopathy could constitute an 1980; Kalia et aI., 1985a,b). interesting model of Creutzfeldt-lakob disease. In these species, an acute knowledge of catecholaminergic 1. 1. Caudal medulla oblongata neurons is essential to understand these regulations. In all neuroanatomical studies and particularly in 1.1 .l.Al cell group those concerning catecholamine-containing neurons, the delay between death and tissue fixation is critical: the In the rat, the majority of TH-ir and DBH-ir neurons shorter the postmortem delay, the better the preservation are restricted to a small area of the VLM caudal to the of the structures. Under slaughter conditions, especially, area postrema. They extend up to the spinomedullary it is sometimes difficult to perform brain perfusions in junction. These cells, which do not show PNMT large animals (cow or pig). In such conditions quality of immunoreactivity, are thus believed to be noradrenergic. the tissue is very low and the demonstration of catechol We have noted the similar distribution patterns of such amine molecules is difficult either using formaldehyde cells in the cat and primate homologous region. induced fluorescence or immunohistochemistry with However, such presumptive noradrenergic neurons are antibodies raised against dopamine or noradrenaline. less in number in the ungulate VLM, and are not However, using immunohistochemistry of catechol detectable in the sheep spino-medullary junction. amine-synthesizing enzymes, it becomes possible to study their distribution in brain tissues of several species 1.1.2. A2 cell group of farm animals (Tillet, 1988; Tillet and Thibault, 1989; Ostergaard et aI., 1992; Ruggiero et aI., 1992; Kitahama ]n the rat and cat, TH- and DBH-ir neurons, which et aI., 1994; Leshin et aI., 1995a,b, 1996). Antibodies are not immunoreactive for PNMT, are concentrated in raised against the enzyme of catecholamine synthesis the commissural subnucleus (of the nucleus of the (phenylethanolamine-N-methyl transferase, PNMT; solitary tract (NTS» and extend up to the s pino dopamine-beta-hydroxylase, DBH; aromatic L-amino medullary junction, where they are present mainly acid decarboxylase, AADC or tyrosine hydroxylase, TH) around the central canal. In the human commissural were used to detect adrenergic, noradrenergic and region, they are scattered through the nucleus. ]n dopaminergic neurons, respectively. In this short review, ungulates, at least in sheep and cattle, they are far lower we present the main characteristics of the distribution of in number in the dorsal vagal complex and do not extend catecholaminergic neurons in large breeding animals more caudally. compared to their organization in human, monkey, cat and rat. As a common frame, we used the nomenclature of 1.2. Rostral medulla oblongata catecholamine neuronal group previously determined in rats by Hokfelt et al. (1984b), although many differences 1.2.1. Cl and rostral Al cell groups exist between the brains of rats, ungulates and primates. Catecholamine neuronal structures were described from In the rat (Fig. lA), rostrally situated TH/DBH-ir caudal to rostral levels. cells which also contain PNMT, form a compact aggregate mainly in the lateral paragigantocellular 1. Medulla oblongata nucleus (PGCL) (Hokfelt et aI., 1984a), and some extend dorsally in the reticular formation. Such cells are defined Catecholaminergic neurons in the medulla oblongata as the Cl group as mentioned above. are believed to play an important role in autonomic In other species, such as carnivores, ungulates and regulation, such as cardiovascular, respiratory and primates, we found several important species differences general visceral controls (Tork et aI. , 1990). Morpho in cell organization when compared with rodents, as we logically, they were first demonstrated by Dahlstrom and describe below. Fuxe (1964) to display green histofluorescence in the rat, In the cat brain (Fig. IB), TH- and DBH-ir cells are and to be distributed through the entire extent of the concentrated in the VLM dorsal to the lateral reticular medulla. These authors classified them into two groups, nucleus, but many are dispersed more dorsally in the Al and A2; Al cells were clustered in the ventrolateral reticular formation (equivalent to the rat intermediate medulla (VLM) and A2 cells were concentrated in the reticular nucleus according to Paxinos and Watson, dorsomedial medulla.

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