14.2 Pineal and reproduction
14.3 Pineal secretions
14.4 Pineal and gonadal activity
14.5 Role of pineal in the regulation of reproductive cycles
The pineal organ shows considerable anatomical diversity among the various species of Vertebrates which is evident at all levels from gross morphology to the ultrastructure of the constituent cells. The pineal complex in fishes is generally composed of a hollow pineal vesicle and a pineal stalk which is associated with habenular ganglia, habenular and posterior commissures and sub-commissural organ. The pineal vesicle contains three morphologically distinct cell types: the sensory cell, the supporting cell, and the ganglion cell. Of these, the sensory cells are the most abundant (Holmgren, 1959) and are chiefly located in the vesicular area on the sides of the lumen (Hafeez and Ford, 1967). The sensory cells have an outer and an inner segment, the former has numerous membranous saccules while the latter often has dense particles, mitochondria and oil droplets. A sensory cilium (connecting piece) extends from the inner segment and gives rise to membranous saccules comprising the outer segment. Electron microscopic studies also suggest a photoreceptive function for the pineal organ of fishes (Takahashi and Kasuga, 1971); Oguri and Omura, 1973; Urasaki, 1976). Further the photosensory cells of the teleost pineal have been shown to be similar to the ciliary type of photosensory cells present in the retina and possess cone-like characteristics (Breucker and Horstmann, 1965; Oksche and Kirschstein, 1967).
Though the pineal organ in fishes has long been a subject of research and review, little is known about its physiology (Fenwick, 1970a; Hafeez, 1971). It is generally believed that in fishes the pineal has a photosensory or photoreceptive function (see reviews by Holmgren, 1959, 1965; Kelly, 1962; van de Kamer, 1965) though some authors (Hafeez and Ford, 1967; Rizkalla, 1970; Hafeez, 1971) have also attributed a secretory function to the pineal organ, Most morphological studies on the teleost pineal suggest a dual sensory and secretory function to this organ (for reviews see Fenwick, 1970a; Hafeez, 1971; de Vlaming, 1974).
Investigations of Hafeez, Wagner and Quay (1978) have revealed differential responsiveness of various pineal cells to environmental lighting; the supporting cells are influenced only by the photic input from lateral eyes, while receptor cells are responsive to incident light input through the pineal region. That the pineal serves a photosensitive function in teleost fishes is suggested by observations on light-mediated behaviour of fishes and by experiments on phototactic and chromatophore responses as also by electrophysiological studies (Dodt, 1963; Fenwick, 1970a; Morita and Bergmann, 1971).
In recent years, data have fast accumulated to implicate the teleostean pineal in several physiological control mechanisms, especially in responses to photoperiod (de Vlaming, 1975a, b; Delahunty, Schreck and de Vlaming, 1977; Delahunty et al., 1978; Olcese and de Vlaming, 1977; de Vlaming and Vodicnik, 1978; Vodicnik et al., 1978). Pinealectomy induces changes in plasma osmolarity and electrolytes (Weisbart and Fenwick, 1966; Fenwick, 1970c; de Vlaming et al., 1979), and plasma cortisol levels in goldfish (Delahunty, Schreck and de Vlaming, 1977)":
Limited investigations have been conducted on the possible role of the pineal organ in influencing circadian locomotory rhythms in fishes (Fenwick, 1970a; Delahunty et al., 1978; Matty, 1978; Kavaliers, 1979; Sundararaj and Garg, 1980).
Hydroxyindole-0-methyl transferase (HIOMT) which catalyzes the conversion of N-acetyl serotonin to melatonin has been demonstrated in the pineal as well as the. brain of some species of fishes (Quay, 1965; Owman and Rüdeberg, 1970; Smith and Weber, 1974, 1976a, b). The pineal of teleost fishes has been assumed to be independent of retina, unlike in mammals where it is innervated by sympathetic nerves and receives photic input from eyes (Wurtman, Axelrod and Kelly, 1968). In rainbow trout, HIOMT and melatonin levels show diurnal fluctuations with highest levels in the scotophase portion of the light-dark cycle (Smith and Weber, 1976b; Gern, Owens and Ralph, 1978a, b). However, trout retina contains melatonin in highest concentrations during the photophase portion of the light-dark cycle and pinealectomy disturbs neither the rhythm nor the titer of retinal melatonin (Gern, Owens and Ralph, 1978b). Further, blinding abolishes the photoperiod-induced HIOMT cycles in the pineal of rainbow trout, whereas capping of the pineal to direct illumination does not affect these cycles (Smith and Weber, 1976b). According to Fenwick (1970d) the phototactic response of goldfish is dependent upon the presence of the pineal as well as eyes.
Pineal melatonin has been suggested to possess antigonadal properties in a number of vertebrate species (see Minneman and Wurtman, 1976). It can induce marked changes in neuroendocrine and gonadal activities in a number of fishes (Fenwick, 1970b; Urasaki, 1972a, 1977; de Vlaming, Sage and Charlton, 1974; Sundararaj and Keshavanath, 1976; Saxena and Anand, 1977).
Recent studies have demonstrated that melatonin has progonadal properties also and that it inhibits the antigonadal activities of the pineal (Reiter et al., 1975). This ambivalent action of melatonin depends on dose, mode and time of administration, and the photoperiod to which the experimental animals are exposed. However, all the observed antigonadal activities of the pineal extracts cannot be explained by its melatonin content. Therefore, it has been suggested that the pineal may contain several other antigonadotropic substances (see Benson et al., 1976; Ebels, 1976) in the form of some unidentified proteins and polypeptide hormones. Injections of arginine vasotocin (AVT) inhibit compensatory ovarian hypertrophy and prolong the diestrus in the mice (Vaughan and Blask, 1978). Recently, Holder et al. (1979) have reported the existence of AVT in the pineal of teleost fishes.
The available evidence indicates that in teleost fishes the pineal organ plays an important role in the regulation of several physiological processes including reproduction (see Fenwick, 1970a; de Vlaming, 1974; Matty, 1978; Ralph, 1978a, b).
Effects of pinealectomy on reproduction in teleost fishes vary considerably with the species, season and conditions of photoperiod. Krockert (1936a, b) was the first to propose that the. pineal exerts an inhibitory influence on the reproductive function. Schonherr (1955) in Gasterosteus aculeatus, Rasquin (1958) in Astyanax mexicanus. Pang (1967) in Fundulus heteroclitus, and Peter (1968) in Carassius auratus, failed to detect any effect of pinealectomy on gonads. Investigators, more often than not, have not mentioned the photo-period conditions, the time of the year when experiments were conducted, the gonadal maturation stage at the end of the experiment and whether or not gonadal activity was stimulated under laboratory conditions. The importance of such information has been emphasized by Fenwick (1970a, b, c), Urasaki (1972a, b, c), de Vlaming (1975a) and de Vlaming and Vodicnik (1977, 1978). Gonadal regression ensues following pinealectomy in recrudescing and mature golden shiners (de Vlaming, 1975a) and goldfish (de Vlaming and Vodicnik, 1978) kept under long photoperiod and warm temperature as well as in sexually recrudescing golden shiner maintained under long photoperiod and low temperatures. In medaka under conditions of long photoperiod, pinealectomy and/or blinding causes gonadal regression (Urasaki, 1972a, 1973, 1976). However, pinealectomy had no effect under short photoperiod in cold (12°C) temperature (de Vlaming, 1975a), whereas pinealectomy accelerated gonadal recrudescence in spring in goldfish kept under short photoperiod at 13°C (Fenwick, 1970c) or at 20°C (de Vlaming and Vodicnik, 1978). Under short photoperiod and warm temperature, gonadal development is accelerated after pinealectomy in both golden shiner and medaka (de Vlaming, 1975a, Urasaki, 1973, 1976). In fishes where increasing daylength and long photoperiod in the spring stimulate gonadal recrudescence (see de Vlaming, 1972a; Peter and Crim, 1979), the pineal as well as the eyes may have a role in promoting gonadal recrudescence under long photoperiods and in supressing gonadal activity under short photoperiods (Hontela and Peter, 1980). Therefore, the pineal organ can be antigonadal or progonadal during different seasons depending on daylength conditions.
An overall review of the functional aspects of the pineal in fishes reveals that the pineal modulates physiological activities to facilitate breeding during the proper season and to prevent, breeding during the unfavourable seasons of the year. Precision in breeding periodicity is an adaptation to synchronize the emergence of fry with the availability of proper food, which itself is subject to cycles of seasonal abundance.