Download The Preoptic Nucleus in Fishes: A Comparative Discussion of

AMER. ZOOL., 17:775-785 (1977).
The Preoptic Nucleus in Fishes: A Comparative Discussion of
Function-Activity Relationships
R. E. PETER
Department of Zoology, University of Alberta, Edmonton, Alberta T6G 2E9, Canada
SYNOPSIS. The electrophysiological characteristics and the afferent inputs to the preoptic
nucleus (PN) in fishes are reviewed. Information from teleosts indicates that PN neurons
can be divided into different classes on the basis of their combined electrophysiological and
anatomical charactenstics. Afferent input to the PN of teleosts has been demonstrated for
the olfactory, optic, trigeminal, and vagus nerves, and the telencephalon and spinal cord.
In teleosts the preoptic region, and the PN within it, are involved in the control of
spawning behavior and the act of spawning. The neurohypophysial hormones (NH) may
play a role in stimulation of the ovarian and oviduct musculature during spawning. The
possible stimuli for NH secretion for osmoregulatory purposes in freshwater bony fishes
are decreased plasma osmolality, or decreased concentration of some ion in the plasma, or
expansion of either the extracellular or intracellular fluid volume. Decreased blood
volume or blood pressure are also possible stimuli. Receptors on the outside of the animal
may also play a role. Some results suggest that NH may be secreted during stress and that
NH may be involved in stimulation of ACTH secretion in teleosts. In the mammals NH
have some actions on the brain. Vasopressin aids retention of conditioned avoidance
responses in rats. The various stimuli for secretion of NH in fishes and mammals are
compared.
than about that of the fishes, the mammalian literature is used as a model for
Most of the contributions to this sym- comparison and the basis for speculation
posium deal specifically with actions of the with regard to the fishes.
neurohypophysial peptides. In this paper I
will diverge from this theme somewhat to
BONY FISHES
discuss the preoptic nucleus-neurohypophysial system of fishes more in terms of its Electrophysiological activity of the preoptic nuneurophysiological activity. The intention cleus
of the discussion is not to present
neurophysiological information per se, but
The classical electrophysiological study
to try and relate what is known about the by Kandel (1964) on the preoptic nucleus
neurophysiology of the system with the (PN) of goldfish demonstrated that the
physiological actions of the hormones behaviour of neurosecretory neurons is
produced by the system. This topic leads generally similar to that of other central
itself to actions of the hormones on the neurons. Recordings by Kandel were innervous system, making it difficult to sepa- tracellular from the large PN cells belongrate neurophysiology from actions of the ing to the pars magnocellularis. Extension
hormones. A great deal of literature is of the axons into the pituitary was
available on the neurophysiology of the confirmed in 60% of the cells by antidrommagnocellular neuroendocrine system of ic stimulation by an electrode implanted in
mammals and many excellent reviews have the pituitary gland. Such antidromically
appeared recently on this topic (see Cross, identified neurons are supposedly endoI974a,b; Cross and Dyball, 1974; Cross et crine in function. The cells were found to
al., 1975; Hayward, 1972, 19746). It is not have low rates of spontaneous firing. The
my intention to review this literature again presence of inhibitory recurrent collaterals
here. However, because there is much was shown by antidromic stimulation. This
more known about the mammalian system provides a self-imposed system to decrease
INTRODUCTION
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R. E. PETER
or damp out activity, and raises the question of neurotransmitter actions by the
neurohypophysial peptides. Kandel also
found that stimulation of the olfactory
tract produced excitatory postsynaptic potentials and spikes in the PN neurons.
Membrane hyperpolarization and inhibition of spontaneous firing activity occurred with perfusion of the mouth and gills
with sea water diluted 100:1 with tap water. The response in the PN to mouth-gill
perfusion with dilute sea water suggests
some inhibitory input to the PN from such
possible cranial nerves as the vagus, glossopharyngeal, facial or trigeminal. The
specific origin of the input was, however,
not identified.
Hayward (1974a) extended the electrophysiological studies on the PN magnocellular neurons of goldfish to demonstrate the presence of three morphologically and electrophysiologically different
cell types. The cells recorded from were
antidromically identified and stained by
electrophoretic injection of Procion Yellow
via the intracellular recording electrode.
Each cell type was found to have many fine
dendritic branches within the PN itself.
One cell was found to have more extensive
dendritic branches laterally and to receive
olfactory input, and another was found to
have a special extension to the ependyma
that in some cases actually made contact
with the cerebrospinal fluid. Also, Hayward found evidence for invasion of the
pituitary by multiple axon branches from
some PN neurons.
The general excitatory effect of olfactory afferents to the PN has been
confirmed in goldfish by Jasinski et al.
(1967), and Hayward (1974a), and in the
goose fish by Bennetts al. (1968). Bennett
and co-workers (1968) also found excitatory input from the trigeminal nerve. Also,
after transection of the goose fish brain
just posterior to the hypothalamus there
was increased electrophysiological activity
in the PN, suggesting some tonic inhibitory
input from lower brain regions.
Electrical stimulation of different regions of the telencephalon and simultaneous extracellular unit recording in the PN
pars parvocellularis of the sunfishes
Lepomis macrochirus and L. gibossus, demon-
strated that PN cells can be activated by
wide regions of the telencephalon (Hal\ow\tzet al., 1971). Unfortunately the units
recorded were not identified as being en- •
docrine neurons by antidromic activation
by pituitary stimulation. However, the
input from wide regions of the telencephalon does imply that a wide variety of sensory modalities could affect activity of PN
neurons.
As a somewhat unique means to demonstrate activity of PN neurons it was found
by Jasinski et al. (1966, 1967) and
confirmed by Peter and Gorbman (1968)
that electrical stimulation of the olfactory
tracts of goldfish leads to depletion of
paraldehyde fuchsin stainable neurosecretion in the cell bodies and axons of the PN.
Thus, electrical activity of PN neurons is
associated with some change in their special staining characteristics. Similar results
have been observed following olfactory
tract stimulation of Heteropneustes fossilis
(Prasada Rao, 1970) and Clarias batrachus
(Prasada Rao and Dabhade, 1973), and
after stimulation of the olfactory mucosa
of Ophiocephalus punctatus (Chandrasekhar
and Chacko, 1970). In addition, Peter and
Gorbman (1968) found depletion of stainable neurosecretion in the goldfish PN
following electrical stimulation of the retina, tenth cranial nerve, and spinal cord,
demonstrating the existence of functional
afferents to the PN from these sources as
well. Stimulation of the lateral line nerve
and the pineal stalk were without effect,
however. Bennett et al. (1968) found that
spike activity in the pituitary stalk of the
goose fish was increased by stimulation of
the spinal cord, and the trigeminal, optic,
or olfactory nerves. Assuming the activity
recorded in the stalk was due to the PNneurohypophysial system, these results
support the findings of Peter and
Gorbman (1968). In summary, the PN
obviously has a wide range of afferents
from which it can receive input.
A ctivity-function relationships
Involvement of neurohypophysial hormones in spawning behavior of the kil-
PREOPTIC NUCLEUS ACTIVITY IN FISHES
lifish, Fundulus heteroclitus, was proposed
by Wilhelmi et al. (1955) when it was discovered that intraperitoneal injection of
large doses of neurohypophysial hormone
» preparations induced a "spawning reflex
response." A full reflex response is described as an S-shaped flexure of the body,
simultaneous with quivering of the body
and flattening of the anal and dorsal fins to
one side, ending with a quick and vigorous
flick of the tail that darts the animal forward (Macey et al., 1974). This response
can be elicited in killifish of either sex
(Wilhelmi et al., 1955), after castration
(Pickford, unpublished observations cited
by Wilhelmi et al., 1955), or hypophysectomy (Pickford, 1952). A similar spawning
reflex response occurs in response to
exogenous neurohypophysial hormones in
some closely related cyprinodontiform
species: Oryzias latipes (Egami, 1959) and
Gambusia sp. (Ishii, 1963). However, such a
response is not elicited in the less-closely
related cypriniforms: Carassius auratus
(Pickford, unpublished results cited by
Macey et al., 1974), Misgurnus fossilis
(Egami and Ishii, 1962), and Heteropneustes
fossilis (Sundararaj and Goswami, 1966).
The PN has been directly implicated in
the spawning reflex response off. heteroclitus by Macey et al. (1974). They found that
complete or nearly complete destruction
of the PN by electrolytic lesioning
abolished or nearly abolished the reflex
response to exogenous neurohypophysial
hormone preparations, including the native hormone arginine vasotocin (AVT). If
the lesions left more than about 6.5% of
the PN cells intact, the response occurred
at about a similar rate as in the sham
control animals. Lesioning of a number of
other forebrain regions also had no effect
on the response. These results suggest
involvement of the PN in spawning behavior of the killifish. As a mechanism to
explain the occurrence of the spawning
reflex response, Macey et al. (1974)
suggested that activation of the PN was by
action of the injected hormones on some
brain center, perhaps directly on the PN
itself.
To test the effects of direct brain injection of neurohypophysial hormones on
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spawning reflex behavior, a technique was
developed by Peter and Knight (unpublished results) to chronically implant a
cannula in the third ventricle of the brain
of the killifish. In unpublished results by
Pickford and Knight (personal communication) it was found that brain injection of
an estimated dose of 5 mU arginine vasopressin (AVP)/g body weight gave no response in five trials. Injection of a higher
dose, estimated at 100 mU/g body weight,
gave a positive response in 5 out of 19
trials. Since the dose required to elicit a
response by brain injection is similar to
that required intraperitoneally, it seems
likely that those fish that responded following a brain injection did so as a result of
some peripheral action of the hormone.
This situation is not likely a problem of
specificity of the hormone used because
large doses of AVT are also required when
injected intraperitoneally. Furthermore, in
view of the large doses normally required
to elicit a spawning reflex response it
seems that activation of a peripheral receptor by neurohypophysial hormones is
probably not a part of the normal
mechanism for triggering spawning behavior in teleosts.
Given the above situation, does the PNneurohypophysial system have any role in
spawning behavior in teleosts? Demski and
Knigge (1971) observed that electrical
stimulation of the preoptic region evoked
courtship behavior in the male bluegill
sunfish (L. macrochirus). In some cases in
which a female was available for the stimulated male, actual spawning took place
(Demski, personal communication). Nest
building in the bluegill is evoked by stimulation of the dorsal area of the telencephalon (Demski and Knigge, 1971), suggesting
that some aspects of the full sphere of
reproductive behavior are not centered in
the preoptic region. As mentioned previously, destruction of the PN abolishes the
spawning reflex response of killifish
(Macey et al., 1974). As a further demonstration of the involvement of the preoptic
region in spawning, Demski et al. (1975)
have shown by electrical stimulation and
lesioning experiments on male green
sunfish (L. cyanellus) that a pathway to
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R. E. PETER
evoke semen discharge originates in the
preoptic region, and traverses lower brain
regions into the rostral spinal cord. Unpublished observations by Demski, Bauer
and Gerald (cited by Demski et al., 1975)
indicate that sperm release in spermiated
male goldfish and discharge of ovulated
eggs in female goldfish may also be evoked
by preoptic stimulation. Together all of
these observations implicate the preoptic
region in the act of gamete discharge during spawning and in spawning behavior of
teleosts, but these results do not imply a
role of the neurohypophysial hormones in
this system. The possible involvement of
the endocrine neurons of the PN would
then be by their synaptic interconnections
with other neurons rather than by their
endocrine function.
In spite of the above denials, a possible
means for involvement of the neurohypophysial hormones in spawning may be via
the abilities of the hormones to stimulate
activity of oviduct and ovarian smooth
muscles in teleosts (see Heller, 1972;
LaPointe, 1977). Thus, the neurohypophysial hormones may serve as a part of
the efferent system in spawning to accomplish stimulation of the oviduct and
ovarian musculature, and perhaps also the
sperm duct musculature, although there is
no information available concerning the
latter.
Stacey and Liley (1974) demonstrated
that an intra-ovarian mass of ovulated eggs
must normally be present in order for
female goldfish to show spawning behavior. On the other hand, spawning behavior can be induced in female goldfish in
the absence of ovulated eggs by intraperitoneal injection of a large dose of
prostaglandin F ^ (Stacey, 1976). Stacey
also found that the spawning behavior
usually induced by injection of ovulated
eggs into the ovipore could be blocked by
intraperitoneal injection of indomethacin,
a blocker of prostaglandin synthesis.
These results imply an effect of ovulated
eggs, perhaps on the ovary or oviduct, to
cause prostaglandin release which would
in turn somehow initiate afferent stimuli
involved in triggering spawning behavior
in goldfish. At least a part of this afferent
stimulus system involves the pituitary
gland. Stacey (1976) found that hypophysectomy abolished the ability of
PGF^ to induce spawning behavior in
female goldfish, and that the behavior was
restored by injection of a purified salmon
gonadotropin preparation. This implicates
gonadotropin as the particular pituitary
factor involved in the afferent stimulus
system. However, where and how gonadotropin acts is an open question. Of
course stimuli other than those indicated
above also impinge on this circuit, including such factors as the presence or absence
of a mate and environmental conditions.
For example, a pheromone from ovulated
eggs and ovarian fluid of ovulated goldfish
that attracts and induces spawning behavior in spermiated males has recently
been demonstrated (Partridge et al., 1976).
For all the various stimuli involved in
evoking spawning behavior, the telencephalon may play an integrative role.
This would particularly be true of olfactory information. Destruction of large
amounts of the telencephalon, including
total destruction, have, in fact, been noted
to cause a marked decline or even extinction of certain aspects of reproductive behavior (see Aronson, 1970; Aronson and
Kaplan, 1968). However, the major role of
the telencephalon in fishes with regard to
various behaviors is hypothesized to be
more as an activator (Aronson, 1970;
Aronson and Kaplan, 1968), rather than as
an integrator. Unfortunately, the relationships between the telencephalon and
preoptic region in the forebrain ablation
experiments received little attention.
Thus, for the moment it is assumed that
the preoptic region is the main integrator
for spawning behavior. If this were true it
would complete the circuit of afferentefferent activity in relation to spawning
behavior and egg and sperm release.
A tentative model, encompassing all of
the foregoing, to explain spawning and
spawning behavior in female oviparous
teleosts is shown in Figure 1. Not shown in
the model is the possible action of the sex
steroids or other hormones in priming the
animal for reproductive behavior (see
Liley, 1969, 1972; Liley and Wishlow,
PREOPTIC NUCLEUS ACTIVITY IN FISHES
SPAWNING BEHAVIOR
FIG. 1. A tentative model describing the control of
spawning and spawning behavior in an oviparous
female teleost. Evidence for the various elements
incorporated in the model are described in the text.
1974). Presumably the action of the sex
steroids is on the brain, but the site of
action has not yet been explored.
In freshwater adapted bony fish, including the lungfish, the neurohypophysial
hormones, particularly AVT, function as
diuretic hormones (see Maetz and Lahlou,
1974; Pang, 1977; Perks, 1969; Sawyer,
1972; Sawyer and Pang, 1975) and possibly to stimulate sodium uptake by the gill
(Maetz and Lahlou, 1974). Related to these
actions are the vasopressor effects of the
hormones, specifically to cause increased
pressure in the dorsal and ventral aorta
and the shunting of blood in the gill (see
Chan, 1977; Maetz and Lahlou, 1974).
The receptors that might subserve activation of the PN in relation to these functions may be located externally or internally. Extero-osmoreceptors may serve to
detect changes in osmotic pressure or ion
concentration changes of the external
medium. The finding by Kandel (1964)
that perfusion of the mouth and gills of
goldfish with dilute sea water causes inhibition of activity in PN neurons suggests a
mouth-gill location. The inhibition of PN
activity and presumably concomitant decrease in secretion of hormone is a seemingly functional response in view of the
osmoregulatory actions of the hormones.
779
On the other hand, perfusion of the olfactory epithelium of goldfish with NaCl solutions of various concentrations stimulates
activity in the olfactory bulb and telencephalon (e.g., Hara and Gorbman, 1967;
Oshima and Gorbman, 1966), and can also
stimulate the activity of PN neurons in
goldfish (Jasinski et al., 1967). Since activation would supposedly be associated with
secretory activity of the PN-neurohypophysial system, it is difficult to resolve the
functional significance of this response in
terms of the osmoregulatory actions of the
hormones. However, perfusion of the olfactory mucosa of a goldfish with NaCl
solutions ranging from 10~2 M to 5 x
10~2 M (Hara and Gorbman, 1967) may be
considered a general irritative stimulus,
and not comparable to the sort of stimulus
the goldfish might normally encounter.
At this point there is no direct evidence
for entero-osmoreceptors. However, indirect evidence for such receptors is provided by the observations that goldfish
(Rourget etal., 1964) and lungfish (Sawyer,
1972) are able to compensate for intraperitoneal water and salt loading. As
hypothesized by Sawyer (1972), the receptors could cue specifically to either a decrease in plasma osmolality or a decrease in
concentration of a particular ion, such as
sodium, or expansion of the extracellular
fluid volume. Yet another possibility is that
the receptors could cue to expansion of the
intracellular fluid volume or osmoreceptor
expansion. Expansion of the intracellular
fluid volume would also occur with sodium
depletion due to a shift of water to the
intracellular space. These various possibilities and the supposed AVT secretion
are illustrated in Figure 2.
There are some suggestions that
neurohypophysial hormones have involvement in stimulation of adrenocorticotropin (ACTH) secretion during stress
responses in teleosts. Hawkins and Ball
(1973) found that injection of arginine
vasopressin into the molly, Poecilia
latipinna, with an autotransplanted pituitary caused increased ACTH release.
Stressful conditions, such as electric fishing
and abrupt temperature or salinity
changes, were noted to cause depletion of
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R. E. PETER
Absoluu hydration
ECF
ICF
dehydration
ECF
—+• AV7+*
ing, parturition, or other reproductive activities of elasmobranchs.
ICF
N.j
CYCLOSTOMES
^ N ,
depletion
Normal ulanc*
Similar to the elasmobranchs no electrophysiological studies have been done on
activation of the PN-neurohypophysial system in cyclostomes. However, exposure of
larval lampreys to continuous light causes
depletion, whereas continuous dark causes
accumulation, of stainable neurosecretion
in the cell bodies and axons of the PN
N.+
(Oztan and Gorbman, 1960). This suggests
that afferents to the PN may come from
FIG. 2. A speculative scheme showing the changes light receptors located somewhere. No
in extracellular fluid volume (ECF), and intracellular further studies have been done on the
fluid volume (ICF) of enteroosmoreceptors in a
freshwater teleost. The changes in osmotic balance mechanisms of activation of the PN in
causing the alterations in ECF and ICF are given for cyclostomes.
ECF
ICF
»> AVT»
dohydratton
Rtlativ hydration
ECF
ICF
ICF
ECF
each situation, along with the supposed changes in
arginine vasotocin (AVT) secretion.
COMPARISON WITH THE MAMMALIAN MODEL
stainable neurosecretion in the PN of the Electrophysiology
European eel by Leatherland and Dodd
The mammalian homologue of the
(1969). Obviously further research is required to understand the role of the preoptic nucleus in fishes is the supraoptic
neurohypophysial hormones in stimulat- nucleus (SON) and the paraventricular
ing ACTH secretion and the response of nucleus (PVN). In those mammals (cat,
the PN-neurohypophysial system during rat, rabbit, monkey) on which electrophysiological studies have been done,
stressful situations.
no exceptional characteristics of the SON
and
PVN neurons have been found (see
CARTILAGENOL'S FISHES
Cross I974a,b; Cross et al, 1975; Hayward,
The electrophysiological characteristics 1972, 19746). As in the teleosts, the mamof PN neurons in elasmobranchs have not malian magnocellular neuroendocrine
been studied. Likewise there is no infor- cells, identified as such by antidromic actimation available on the functional vation by pituitary stimulation, generally
mechanisms of activation of the PN. Un- have low rates of spontaneous activity.
fortunately, even the functions of the Also similar to the teleosts is the evidence
hormones are poorly defined (see Maetz for inhibitory recurrent collaterals in some
and Lahlou, 1974; Perks, 1969). Neurohy- antidromically identified SON and PVN
pophysial hormones have been shown to neurons. Different from teleosts, however,
have some ability to stimulate contraction is the finding of a significant portion
of oviduct muscle in the dogfish (~20%) of neurons that have bursts of
Scyliorhinus caniculus (Heller, 1972). This firing alternating with silent periods.
may imply the presence of some sort of
There have been no attempts to date to
afferent input from the ovary and oviduct correlate electrophysiological activity of
to the preoptic region, as is supposedly PN neurons in fishes with various suppresent in teleosts. However, since the posed states of secretory activity. However,
reproductive process is so poorly under- much effort has been devoted to this in
stood in elasmobranchs (see Dodd, 1975) mammals and a general correlation obit is highly tenuous to suggest a role of the tained (see Cross, 19746; Crossed al., 1975;
PN-neurohypophysial system in egg lay- Hayward, 1972, 19746). For example, in
PREOPTIC NUCLEUS ACTIVITY IN FISHES
response to dehydration by substitution of
a 2% NaCl solution for drinking water
there is increased firing activity of rat SON
and PVN neurons (Dyball and Pountney,
1973). The more direct, but perhaps more
artificial, stimulus of intracarotid infusion
of hypertonic saline or glucose solutions
also causes increased firing activity of cells
in and around the SON of the monkey (see
Hayward, 19746). The PVN and SON
neurons that show spontaneous bursting
seem to be related to oxytocin release
(Cross 1974a,b; Cross et al., 1975; Lincoln
and Wakerly, 1974, 1975). During suckling in rats the bursting neurons specifically
show increased burst frequency and more
spikes per burst. This activity correlates
with increased intramammary pressure
and milk ejection. However, the bursting
neurons of rats (Dyball and Pountney,
1973) and monkeys (Hayward, 1974ft) also
show increased activity following intracarotid saline infusion. Thus, classification of the neurons as being vasopressinor oxytocin-secreting is difficult on the
basis of electrophysiological findings.
A ctivity-function relationships
The actions of oxytocin on the uterine
smooth musculature in mammals and the
actions of neurohypophysial hormones on
the oviduct and ovary musculature in
fishes (see above) are analogous systems.
Thus, although the neural pathways involved in oxytocin release in mammals
have been investigated (see Cross and
Dyball, 1974), a strictly homologous afferent and efferent system for the release of
neurohypophysial hormones to stimulate
oviduct and ovarian muscles in fish is unlikely. For reproductive behavior in
mammals, the preoptic region has been
implicated as a hormone-sensitive center
that must be intact and primed by the sex
steroids in order for the behavior to occur
(see Lisk, 1973). This is similar to what we
know about teleost fishes (see above), except that the role of the sex steroids in
priming the preoptic region or some other
brain region has not been explored. A
major difference between the teleosts and
mammals is that in the fishes the mag-
781
nocellular neuroendocrine system is apparently encompassed in the part of the
preoptic region involved with spawning
behavior. In the mammals there are no
indications that the magnocellular neuroendocrine system is involved in reproductive behavior.
The osmotic stimuli for neurohypophysial hormone secretion in the freshwater
bony fishes (see above) are in general opposites to the stimuli for vasopressin secretion in mammals. Increased osmolality of
the plasma due to saline infusion or dehydration by water deprivation, or infusion of hypertonic saline into the brain
ventricular system all provide a hypertonic
stimulus to evoke vasopressin secretion in
mammals (see Anderson, 1972; Hayward,
1972; Moses and Millar, 1974; Share
1974). Each of these situations is associated
with increased extracellular sodium concentration, although a change in sodium is
not a necessary requisite for the osmotic
stimulus. What seems to be the common
element and may be the mechanism for
detection of these osmotic stimuli is a decreased intracellular fluid volume, or supposed decrease in osmoreceptor volume.
The osmoreceptors involved in detection
of these changes may be endocrine
neurons of the SON or PVN (see Cross,
1974ft; Cross et al., 1975; Hayward, 1972,
1974ft). However, it seems more likely that
the osmoreceptors are interneurons in or
adjacent to the SON and PVN since the
cells that respond to osmotic stimuli in
monkeys fall into two classes (Vincent et al.,
1972). One class reacts monophasically
with inhibition or excitation to intracarotid
saline infusion and is not antidromically
activated by pituitary stimulation. The second class responds biphasically to intracarotid saline infusion and is antidromically activated by pituitary stimulation.
However, this categorization is not firm
when other species are considered, because the types of responses to an osmotic
stimulus can be quite varied (see Cross,
1974ft; Cross et al., 1975; Hayward, 1974ft).
The entero-osmoreceptors of freshwater
fishes may, as discussed above, respond to
either a decrease in plasma osmolality, or a
decrease in the plasma concentration of a
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R. E. PETER
particular ion such as sodium, or an increase in the extracellular fluid volume, or
possibly an increase in the intracellular
fluid volume (see Figure 2). The question
of the location and the nature of the
entero-osmoreceptors in freshwater fishes
is open. Unlike mammals, fishes likely
utilize information from extero-osmoreceptors to regulate neurohypophysial
hormone secretion.
Another important stimulus able to
evoke vasopressin secretion in mammals is
hypovolemia (see Hayward, 19746; Moses
and Millar, 1974; Share, 1974). Such a
stimulus occurs in the event of dehydration due to water deprivation, hemorrhage, or decreased blood pressure. While
the first of these stimuli is able to also act
via osmoreceptors, hypovolemia is detected variously by atrial stretch receptors,
and aortic and carotid baroreceptors.
Baroreceptors have been shown to be
present in at least the bony fishes (for
review see Randall, 1970), but involvement
in stimulation of neurohypophysial hormone secretion has not been investigated.
However, it seems likely that decreased
blood volume due to hemorrhage and
perhaps also decreased blood pressure
would serve as stimuli for neurohypophysial hormone secretion in fishes for two
reasons. First, the neurohypophysial hormones have vasopressor effects in the bony
fishes, elasmobranchs and cyclostomes
(see Maetz and Lahlou, 1974). Although
the pressor effects may be more related to
regulation of gill function, as suggested by
Maetz and Lahlou (1974), involvement in
regulation of blood pressure would imply
that the hormones could be released in
response to the appropriate signal to cause
an increase in blood pressure. One such
signal, similar to that seen in mammals,
could be decreased blood pressure and/or
hypovolemia. However, while this seems
logical, it is contrary to the suggestion
above and by Sawyer (1972) that expansion of the extracellular fluid volume may
be a stimulus for neurohypophysial hormone secretion to prevent hydration. The
second means by which hemorrhage may
stimulate neurohypophysial hormone secretion in fishes is by the general stress
response associated with it. In addition to
hemorrhage, some other types of stress
such as loud sounds, pain and intense
emotion have also been found to cause
vasopressin release in mammals (see Cross
and Dyball, 1974; Hayward, 1972). Evidence cited above suggests that at least
some stressors may also cause activity of
the PN-neurohypophysial system in bony
fishes. The release of neurohypophysial
hormones as a result of a handling stress
could also account for the commonly observed "laboratory diuresis" of freshwater
teleosts.
In relation to stress responses of mammals, the corticotropin-releasing hormone
(CRH) activity of vasopressin has received
much attention from researchers in the
past (see Yates and Maran, 1974). At this
point it is established that there is a
hypothalamic CRH separate from vasopressin. Furthermore, the action of vasopressin in stimulating ACTH secretion
seems to be primarily one of potentiating
the action of hypothalamic CRH at the
level of the pituitary (see Yates and Maran,
1974). In the experiments by Hawkins and
Ball (1973) reviewed above it was found
that vasopressin had ACTH releasing ability in the molly. In order to determine if a
homologous system for stimulating ACTH
secretion exists in fishes and mammals,
research will have to be done on fishes
using the native neurohypophysial hormones.
Another sphere of action of oxytocin
and vasopressin in mammals encompasses
effects on the brain. This area is totally
uninvestigated in fishes. In rats and rabbits
it has been found that electrophoretically
applied oxytocin causes excitation of a
major portion of the antidromically identified neurons in the PVN, but that it has
no action on the non-antidromically activated neurons of the PVN or on any
neurons of the SON, thalamus or cerebral
cortex (Moss et al., 1972). Electrophoretically applied vasopressin and intravenous
oxytocin were also ineffective. In a similar
study on cats by Nicoll and Barker (1971) it
was found that electrophoretically applied
vasopressin tended to excite cells in the
cerebral cortex but inhibit antidromically
PREOPTIC NUCLEUS ACTIVITY IN FISHES
identified SON neurons and/or SON
neurons showing recurrent inhibition.
Higher amounts of applied hormone
tended to have reverse effects. Thus, while
these somewhat contrasting results suggest
that the neurohypophysial hormones may
have some transmitter activity, such a conclusion is not warranted without further
investigation. The suggestion from the results by Nicoll and Barker (1971) that
vasopressin may be the agent involved in
recurrent inhibition does not seem tenable
because homozygous Brattleboro rats,
animals unable to synthesize vasopressin,
still display recurrent inhibition (Dyball,
1974).
Neurohypophysial hormones do have
actions on the brain to influence certain
behaviors. Retention of a conditioned
avoidance response is very markedly aided
by injections of Pitressin tannate in oil
(de Wied and Bohus, 1966). This action is
likely due to the vasopressin in the preparation, since subcutaneous injection of a
single dose of lysine vasopressin (1 ng or
0.6 U) aids retention of a conditioned
avoidance response in rats (Bohus et al.,
1974; King and de Wied, 1974; de Wied,
1971). The avoidance behavior is affected
only when the lysine vasopressin is given
within about 1 hour before or after the
training for the avoidance response. The
retention of the avoidance response is up
to a few days whereas saline treated control animals have extinction of the response within two days. Such hormones as
oxytocin, 4~l0ACTH, angiotensin II, insulin or growth hormone do not have a
similar effect. As further support for this
action of vasopressin, homozygous
Brattleboro rats are deficient in learning
avoidance behavior (Bohus et al., 1974).
The important implication from these
studies is that vasopressin can alter the
retention of the long-term memory of certain conditioned avoidance responses. A
lesioning study by Wimersma Greidanus et
al. (1974) indicates that at least some of
the action of vasopressin in this regard
involves the posterior thalamic region,
particularly the parafascicular nuclei.
When lesions were placed in this region
higher doses of vasopressin were required
783
to prevent extinction of the avoidance reresponse; without vasopressin, lesions in
this area accelerate extinction. What other
brain regions may be involved remains to
be determined.
While these experiments clearly demonstrate some actions of vasopressin on a
specific behavior, it is difficult to understand the context within which these results should be viewed. One notable problem with these studies is the very large
dose of hormone usually administered.
Also, lysine vasopressin has been used,
rather than the hormone native to the rat,
arginine vasopressin. Perhaps now that a
brain region associated with the response
has been located, smaller doses of the
native hormone can be given directly into
the brain.
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