Masahiko Satou

Synaptic organization, local neuronal circuitry, and functional segregation of the teleost olfactory bulb

Abbreviations

Telencephalic and preoptic areas integrate sexual behavior in hime salmon (landlocked red salmon, Oncorhynchus nerka): results of electrical brain stimulation experiments

Various patterns of sexual behavior were evoked in freely swimming hime salmon by electrical stimulation of specific loci in the telencephalon and the preoptic area (POA) using chronically implanted electrodes. Furthermore, co-ordinated sexual behavior corresponding to stages of the natural spawning sequence was elicited from some of these brain regions. These results suggest that (1) sexual behavior is integrated in specific parts of the telencephalon and POA, and (2) within these regions there is a hierarchy of neural systems which mediate progressively more complete components of normal sexual behavior.

Descending pathways to the spinal cord in the himé salmon (landlocked red salmon, Oncorhynchus nerka)

Distribution and morphology of the cells of origin of the descending spinal pathways and their axonal courses were studied in the himé salmon, using retrograde labelling with cobaltic lysine and horseradish peroxidase (HRP). Following application of the tracers to the cut end of the spinal cord or injection of the tracers at the 10th to 15th spinal segment, neurons mainly labelled via the axons of passage were distributed in the mesencephalon and the rhombencephalon. Mesencephalic cell groups consisted of the nucleus pretectalis, the nucleus fasciculi longitudinalis medialis, and the nucleus ruber. The former two cell groups sent their axons to the fasciculus longitudinalis medialis. The axons of the nucleus ruber formed a separate loose bundle, the “tractus rubrospinalis.” The rhombencephalic cell groups consisted of the rhombencephalic reticular formation, the Mauthner cells (one cell for each side), and the octavolateral area. The rhombencephalic reticular formation could be further subdivided into the nucleus reticularis superior, nucleus reticularis medius, and nucleus reticularis inferior. The axons of these cell groups joined the fasciculus longitudinalis medialis and the “tractus bulbospinalis.” The Mauthner cell had two main gigantic dendrites, and its giant axons formed a conspicuous fiber of Mauthner throughout the rhombencephalon down to the spinal cord. The octavolateral area could be subdivided into the nucleus vestibularis magnocellularis, nucleus tangentialis, nucleus vestibularis descendens and nucleus intermedius. The axons of the nucleus vestibularis magnocellularis and nucleus intermedius entered the fasciculus longitudinalis medialis and/or the tractus bulbospinalis. Those of the nucleus vestibularis descendens and nucleus tangentialis formed the “tractus vestibulospinalis”. The descending spinal pathways of the himé salmon were compared with those of other fishes and other vertebrates. The significance of these descending spinal pathways in the control of locomotion and sexual behavior is also discussed.

Involvement of the telencephalic hemispheres and the preoptic area in sexual behavior of the male goldfish, Carassius auratus: a brain-lesion study.

To locate the brain areas involved in sexual behavior, the effects on male sexual behavior of localized electrolytic lesions in various parts of the telencephalic hemispheres and the preoptic area and of gross ablations of parts of the telencephalic hemispheres were examined in goldfish. All three patterns of male sexual behavior examined (following, butting , and spawning) were severely impaired after bilateral lesions confined to the area ventralis telencephali pars supracommissuralis and/or posterior parts of the area ventralis telencephali pars ventralis (Vs- pVv ), the nucleus preopticus periventricularis (NPP), the lateral forebrain bundle ( LFB ), or the medial forebrain bundle (MFB). On the other hand, sexual behavior was almost unaffected after bilateral ablations of the anterior part or lateral and dorsal parts of the telencephalic hemispheres (AT or LT-DT). Bilateral lesions confined to the area ventralis telencephali pars dorsalis (Vd), the area ventralis telencephali pars postcommissuralis (Vp), the area dorsalis telencephali pars centralis (Dc), the nucleus preopticus (NPO), or the lateral preoptic area (LPA) also had almost no effect on sexual behavior. These results indicate that a particular site in the ventral part of the telencephalic hemispheres (Vs- pVv ) and the anterior part of the preoptic area (NPP) play important roles in the sexual behavior of male goldfish. It was suggested that facilitatory influences from these areas are transmitted through the LFB and/or the MFB.

Central nervous system control of osmoregulation in the eel (Anguilla japonica)

Abstract 1. 1. Participation of the central nervous system in teleost osmoregulation was studied using cultured Japanese eel, Anguilla japonica . 2. 2. Removal of the telencephalon had no effect on survival and plasma ion concentrations either in fresh water or in sea water. 3. 3. “Decerebrated” eels (with entire prosencephalon and mesencephalon removed) adapted to both fresh water and sea water, and ingested almost the same amount of water as the intact eel during the course of sea-water adaptation. 4. 4. Vagotomized eels died 4–5 days after transfer to sea water, whereas they survived well in fresh water. 5. 5. The drinking rate of the vagotomized eel was about half that of the sham-operated eel on the first day of sea water adaptation and was reduced to about 10 per cent by the third day.

Vibrational communication during spawning behavior in the himé salmon (landlocked red salmon,Oncorhynchus nerka)

SummarySexual behaviors of the salmon are composed of a stimulus-reaction chain, which ensures synchronous spawning between the sexes and successful fertilization. To characterize the signals involved in such a stimulusreaction chain, the body vibration and electromyographic activity of the trunk muscles during spawning were simultaneously recorded from freely behaving male and female pairs of himé salmon (landlocked red salmon,Oncorhynchus nerkd) and were analyzed in combination with a videographic analysis of behavior sequences. The results showed that the himé salmon have an elaborate communication system in which characteristic vibrational signals are exchanged. These are produced by body vibration due to trunk muscle activity related to spawning and are transmitted between the sexes with an accurate timing through the stimulus-reaction chain. They act as timing cues to synchronize gamete release and are thought to be shared among a wide variety of fishes. It was hypothesized that the lateral line sense is involved in the detection of these vibrational signals. Furthermore, based on the sequence matrix analysis as well as on information theory, intersexual behavioral sequences during spawning were analyzed statistically. The results showed that statistically significant interactions occur between the sexes and statistically significant amounts of information are transmitted through the interactions, supporting the results from recording experiments mentioned above. Characters of the signalling system and possible origins of the vibrational signals are also discussed.

Field potential and intracellular potential studies of the olfactory bulb in the carp: evidence for a functional separation of the olfactory bulb into lateral and medial subdivisions

Summary1.Field potentials in the olfactory bulb and intracellular potentials from mitral cells were analyzed in the carp. Electrical shocks were applied to a part of the input (the lateral or medial bundle of the olfactory nerve: l-ON or m-ON respectively) or output pathways (lateral or medial olfactory tract: LOT or MOT respectively) of the olfactory bulb in order to activate the olfactory bulb partially.2.When shocks were applied to the regions described above, the distributions of the C2-wave component (which reflects the synaptic depolarization of the peripheral dendrites of granule cells) of field potentials were different between the lateral and medial parts of the olfactory bulb. It was suggested that the patterns of excitatory synaptic inputs to peripheral dendrites of the granule-cell population are different between the two parts of the olfactory bulb.3.The distributions of the C3- and C4-wave components (which reflect the synaptic depolarization of somata and deep dendrites of granule cells by volleys in centrifugal nerve fibers to the olfactory bulb) of field potentials were similar between the two parts of the olfactory bulb. It was suggested that the patterns of excitatory synaptic inputs from the centrifugal fibers to somata and deep dendrites of the granule-cell population are similar between the two parts of the bulb.4.Mitral cells activated antidromically by LOT shocks or synaptically by l-ON shocks were located mainly in the lateral part of the olfactory bulb. On the other hand, mitral cells activated antidromically by MOT shocks or synaptically by m-ON shocks were located mainly in the medial part of the bulb.5.Mitral cells, showing IPSPs in response to LOT, MOT and l-ON shocks, but not to m-ON shocks, were located mainly in the lateral part of the olfactory bulb. On the other hand, mitral cells, showing IPSPs to MOT and m-ON shocks, but not to LOT and l-ON shocks, were located mainly in the medial part of the bulb. Such a spatial distribution of mitral cells showing IPSPs was in accordance with that expected from the spatial distribution of the field potentials.6.These results suggest that the olfactory bulb of the carp can be functionally separated into two subdivisions (the lateral and medial parts); the activities of neurons in the one part exert little influence on neurons in the other part.7.From these results we suppose that the olfactory system of the carp is composed of two separate systems; in the lateral olfactory system, the lateral part of the olfactory bulb receives inputs mainly from the lateral bundle of the olfactory nerve and sends outputs to the LOT, while in the medial olfactory system, the medial part of the olfactory bulb receives inputs mainly from the medial bundle of the olfactory nerve and sends outputs to the MOT.

Ganglion cells of the terminal nerve: morphology and electrophysiology

The ganglion cells of the terminal nerve (TN cells) in the carp were identified using intracellular recording and staining techniques. The TN cells showed characteristic location and morphology as well as characteristic responses after electrical shocks to the olfactory nerve and tracts. These features of the TN cells were distinct from those of the mitral or other cells in the olfactory bulb.

An HRP study of afferent connections of the supracommissural ventral telencephalon and the medial preoptic area in himé salmon (landlocked red salmon, Oncorhynchus nerka).

The supracommissural ventral telencephalon and the medial preoptic area have been shown to play important roles in the sexual behavior of himé salmon (landlocked red salmon, Oncorhynchus nerka). In the present study, the sites of neurons projecting to these regions were examined by means of the retrograde horseradish peroxidase (HRP) tracing method. The morphology of neurons in these sites of origin was also studied by means of the Golgi method. The nucleus preopticus periventricularis and the rostral part of nucleus preopticus (NPP-rNPO) received bilateral projections from the middle parts of the area ventralis telencephali pars ventralis (Vv) and the area ventralis telencephali pars dorsalis (Vd), NPP and lateral part of the preoptic area (LPOA), ipsilateral projections from the caudal part of Vv, nucleus anterioris periventricularis (NAPv), nucleus ventromedialis thalami (NVM) at the level of the posterior commissure, nucleus lateralis tuberis pars medialis (NLTm), nucleus anterior tuberis (NAT), nucleus saccus vasculosus (NSV), nucleus recessus posterioris (NRP) and midbrain tegmentum (TG), and a projection from the nucleus posterior tuberis (NPT), which is situated on the midline of the brain. The area ventralis telencephali pars supracommissuralis and neighboring caudal ventral telencephalon (Vs-cV) received ipsilateral projections from almost all parts of the Vv, the middle and caudal parts of Vd, almost all parts of the NNP, the NPO at the level between the habenula and the posterior commissure, and the rostral part of the nucleus dorsomedialis thalami (NDM). The Vs-cV also received a projection from NPT. These findings seem to give anatomical bases for understanding the neural mechanisms involved in sexual behavior as well as neuroendocrine functions.

Sexually dimorphic muscles in the forelimb of the japanese toad, Bufo japonicus

During the breeding season, male anurans display clasping behavior by holding females with their forelimbs. This behavior is peculiar to males, and may require specializations in forelimb musculature. The present study revealed that five kinds of forelimb muscles were heavier in the male Japanese toad than in the female: the flexor carpi radialis (FCR), the flexor antibrachii medialis caput superius (FAMsup), the abductor indicis longus (AIL), the extensor carpi radialis caput superius (ECRsup), and the flexor antibrachii lateralis superficialis caput superius (FALSsup). In addition, one breast muscle, the coracoradialis (CR), was also heavier in males than in females. A quantitative analysis of muscle fibers processed for myosin ATPase activity showed that, in such “sexually dimorphic muscles” of the female, both fast (twitch) and slow (tonic) muscle fibers were of smaller diameter than in other forelimb muscles of both sexes (all male muscles plus “nondimorphic muscles” of the female). Moreover, both types of fibers were less numerous than in the corresponding muscles of the male. These results suggest that the “sexually dimorphic muscles” are used especially for clasping by the male and are degenerative or subnormal in the female. Slow muscle fibers were neither peculiar to, nor abundant in, these clasping muscles, although they may well be necessary for tonic and prolonged contractions of the forelimb muscles during clasping. The mechanism of sexual dimorphism may be a direct action of androgens on clasping muscles or an indirect action on clasping muscles via the innervating motoneurons.