Photosensory Pineal Organ Research Articles

Neural circuits and their structural and chemical reorganization in the light–brain–pituitary axis during parr–smolt transformation in salmon

Salmonid parr–smolt transformation (smoltification) is a transitional stage between freshwater and seawater life when the salmon imprint on their natal stream, change from a territorial feeding behavior to downstream migration, increase their hypoosmoregulatory competence, and change body shape and coloration. Photoperiod is recognized as the most potent initiator and regulator of the smoltification processes. Environmental light signals giving information about photoperiod are conveyed through a light–brain–pituitary axis that encompasses the neural pathways between photoreceptor organs, the brain and the pituitary, and the diurnal rhythm in melatonin secretion by the photosensory pineal organ. In addition, changes in photoperiod may elicit changes in this axis. Employing retinal neural tract tracing and growth associated protein-43 (GAP-43) immunocytochemistry, we provide here new evidence of a structural reorganization in the light–brain–pituitary axis during smoltification. Retinal tract tracing revealed that projections in smolts expand into new territories of the ipsilateral nucleus preopticus parvocellularis pars anterior (PPa) and additional fibers invade deeper into the contralateral PPa and the nucleus preopticus magnocellularis (PM). At this time, GAP-43-immunoreactive cells appear transiently in specific cell groups throughout the brain, but mainly in the olfactory bulb, telencephalon, and hypothalamus. These structural changes in the light–brain–pituitary axis and hypophysiotropic systems are followed by sequential surges of brain neurotransmitters and receptors, and occur prior to the major surges of circulating thyroid hormone and growth hormone levels that are central to smoltification-related processes. Our data point to a specific period of structural reorganization in certain brain circuits, and we hypothesize that these are involved in triggering the subsequent behavioral, endocrine, and physiological changes associated with smoltification.

Spectral sensitivity and mechanism of interaction between inhibitory and excitatory responses of photosensory pineal neurons.

The characteristics and distribution of chromatic-type neurons in the photosensory pineal organ of the river lamprey, Lampetra japonica, were investigated electrophysiologically. Neuronal activity was inhibited by light of short wavelengths and excited by middle to long wavelengths. The maximum sensitivities of the inhibitory and excitatory responses were at about 380 nm and 540 nm respectively. The spike activity of the neurons during steady illumination for a 10-min period was measured. Although a flash of short-wavelength light caused a strong inhibition in the neuron, this effect was not sustained during 10 min of photic stimuli. It was found that the inhibitory effect continued when excitatory (middle-wavelength) light was delivered together with inhibitory (short-wavelength) light. The result supports the hypothesis of photoregeneration in the pineal photoreceptor, which occurs when photoreceptors having high sensitivity to short wavelengths receive middle-wavelength light. Contrary to the inhibitory response, the excitatory one caused by middle wavelengths continued during stimulation. Spike frequency of the neuron was determined by the spectral composition of the light. Since environmental light contains both inhibitory and excitatory components, the neuron would keep both sensitivities during the daytime and could measure the variation in the spectral composition. Judging from the recording sites, the chromatic-type neurons are distributed in the peripheral part of the pineal organ.

Thermal responses of achromatic ganglion cells in the photosensory pineal organ of rainbow trout oncorhynchus mykiss

1. 1. The effect of ambient temperature (thermal response) on the neural activity in achromatic type of ganglion cells was studied in the dark-adapted pineal organ of the rainbow trout, Oncorhynchus mykiss. 2. 2. The discharge rate of ganglion cells increased with increasing temperature. The thermal response could be classified into two types according to the temperatures showing the maximum discharge rate (20.73 ± 1.7°C in type I, 29.12 ± 1.4°C in type II). Above this temperature, the discharge rate decreased and the spikes partly disappeared. The spikes reappeared when the temperature was subsequently decreased. 3. 3. These results suggest that the neural output of achromatic ganglion cells is modulated by the ambient temperature.

Localization of 2-[125I]iodomelatonin binding sites in the brain of the Atlantic salmon, Salmo salar L.

The photosensory pineal organ of teleost fish shows a circadian rhythm in melatonin synthesis, and melatonin is known to influence a number of physiological functions. However, the target sites for melatonin are not known. We have investigated the distribution of melatonin binding sites in the brain of the salmon, Salmo salar. Brains were collected for receptor binding assay and autoradiography at each of three time points: just after lights on, just before lights off, and in the dark at midnight (photoperiod light-dark 12:12, lights on at 08.00 h, lights off at 20.00 h). Specific binding of 2-[125I]iodomelatonin was observed in several brain areas. High densities were associated with (1) the optic tectum, (2) the preoptic area, (3) an area encompassing the magnocellular superficial pretectal nucleus ('nucleus rotundus') and the glomerular complex, (4) the inferior lobes of the hypothalamus, (5) the lateral mesencephalic tegmentum including the torus semicircularis, and (6) the molecular layer of the cerebellum. No binding was observed in the pineal organ or in the pituitary. We observed no differences in labeling between brains collected at different time points, except in the preoptic area where binding was high at 20.00 and 24.00 h, but low at 08.00 h, and in the corpus cerebelli, where labeling in the molecular layer was higher at 24.00 and 08.00 h than at 20.00 h.(ABSTRACT TRUNCATED AT 250 WORDS)

Action of γ-aminobutyric acid (GABA) in the isolated photosensory pineal organ

The effect of GABA (γ-aminobutyric acid), its agonists (muscimol, baclofen) and antagonist (bicuculline) on pineal ganglion cells of the luminosity type were studied in the isolated, superfused pineal organ of the rainbow trout, Oncorhynchus mykiss. Extracellular recordings revealed that GABA added through the superfusion medium caused a clear alteration of the actvity of projecting neurons, which transmit luminosity responses to the brain. Spontaneous discharges of ganglion cells were predominantly suppressed by GABA (33 neurons out of 48), but 10 neurons were clearly excited. Similar effects were observed after addition of muscimol, but not of baclofen. Bicuculline reversed the GABA and muscimol induced inhibition or excitation. In 4 neurons of the luminosity type, GABA caused bidirectional, inhibitory and excitatory responses depending on the state of light- or dark-adaptation. These observations suggest a role of a GABAergic mechanism in the generation and transmission of luminosity responses in the trout pineal organ. It appears that GABA participates in the modulation of light sensitivity during light- and dark-adaptation processes and that this action is mediated by GABA A receptors.

Intracellular responses from UV-sensitive cells in the photosensory pineal organ

A new type of cell having high sensitivity in the ultraviolet (UV) range was found in the pineal organ of the river lamprey, Lampetra japonica, by intracellular recordings. This UV-sensitive cell responded to light with graded hyperpolarizations and had the maximum sensitivity at 380 nm. The response of the cell was much slower than that of the usual pineal photoreceptor with the peak spectral sensitivity at 525 nm. Intracellular injection of Lucifer yellow revealed that the cell consists of 3 parts, corresponding to an outer segment, an inner segment and a terminal of photoreceptor cell. The apical part of the cell protruded into the lumen and the inner segment situated in the layer of photoreceptor cells. It was concluded that this UV-sensitive cell was a UV-specific receptor cell.

Melatonin modulates the neural activity in the photosensory pineal organ of the trout: Evidence for endocrine-neuronal interactions

Hormonal and neural signals transmitted from the pineal organ to the brain in cold-blooded vertebrates presumably convert information about the ambient illumination into signals which may be used to mediate photoperiodic and circadian responses. The possible intrapineal function of melatonin was investigated by recording intra- and extracellularly from photoreceptors and second-order neurons in the isolated superfused pineal organ of the trout (Salmo gairdneri). Melatonin added through the perfusion bath to the explanted pineal organ caused a dose-related and reversible inhibition of ganglion cells of the luminance type whereas the hormone did not significantly affect the membrane potential of photoreceptors and their light-evoked response. The observed effects seem to be independent from photoperiod and adaptation conditions. These results suggest that melatonin provides a feedforward signal to intrapineal neurons regulating the neural output of the organ.

Neural elements in the pineal complex of the frog, Rana esculenta, II: GABA-immunoreactive neurons and FMRFamide-immunoreactive efferent axons

The photosensory pineal complex of anurans comprises an extracranial part, the frontal organ, and an intracranial part, the pineal organ proper. Although the pineal organ functions mainly as a luminosity detector, the frontal organ may monitor the relative proportions of short and intermediate/long wavelengths in the ambient illumination. The major pathway of information processing in the pineal and frontal organs is the photoreceptor to ganglion cell synapse. It is not known whether interneurons form part of the neural circuitry. In the present study, we demonstrate GABA-immunoreactive (GABA-IR) neurons in the pineal and frontal organs of the frog, Rana esculenta. No GABA-IR axons were observed in the pineal nerve between the frontal and pineal organs, or in the pineal tract that connects the pineal complex with the brain. The GABA-IR neurons differed in morphology from centrally projecting neurons visualized by retrograde labeling with horseradish peroxidase. Thus, we suggest that the GABA-IR neurons in the pineal and frontal organs represent local interneurons. Axons of central origin, immunoreactive with a sensitive antiserum against the tetrapeptide Phe-Met-Phe-Arg-NH2 (FMRFamide), were observed in the intracranial portion of the photosensory pineal organ. The immunoreactive axons enter the caudal pole of the pineal organ via the posterior commissure. The largest density of axons was observed in the caudal part, while fewer axons were detected in the rostral portion. The uneven distribution of the FMRFamide-immunoreactive axons may be related to the distribution of different types of intrapineal neurons. FMRFamide-immunoreactive varicose axons were observed in the extracranial frontal organ. A central innervation of the pineal organ, previously known exclusively from amniotes, is probably not per se linked with the evolutionary transition of the pineal organ from a directly photosensory organ to a neuroendocrine organ. It could rather represent a centrifugal input to a sensory system which has been retained when the directly sensory functions have changed, during phylogeny, to neuroendocrine functions.

Electron microscopic analysis of S‐antigen‐ and serotonin‐immuoreactive neural and sensory elements in the photosensory pineal organ of the salmon

Photoreceptor cells in the pineal complex of poikilothermic vertebrates are regarded as homologous with the neuroendocrine pinealocytes in the mammalian pineal organ. They possess an indolamine metabolism, and they contain a number of substances that are immunochemically similar to photo-transduction-related proteins otherwise found in photoreceptors of the lateral eye retina. Using correlative light and electron microscopic pre-embedding immunocytochemistry, we have identified photosensory and neural elements that are immunoreactive with specific antisera against serotonin (5-hydroxy-tryptamine) and the 48 kDa soluble protein S-antigen (arrestin). One type of serotonin-immunoreactive (5HTir) photoreceptor cell was identified. This was characterized by a short basal pole, into which an immunonegative (post-synaptic?) element protruded. Two types of S-antigen-immunoreactive (SAir) photoreceptor cells were observed, one characterized by a short basal pole, similar to that of the 5HTir photoreceptors and the other characterized by a long, extensively branching basal pole. In addition, two types of neurons bearing no morphological specializations typical of photoreceptor cells were SAir: bipolar neurons and multipolar neurons. These were often situated dorsally in the pineal organ. The results indicate an emergence of multiple lines of photoreceptor-derived "pinealocytes" either early in phylogeny, or independently in different taxa. The results are discussed in relation to current theories of pineal evolution.

Intracellular staining of physiologically identified photoreceptor cells and hyperpolarizing interneurons in the teleost pineal organ

The directly photosensory pineal organ of the rainbow trout functions primarily as a luminance detector. Its neutral output reflects the level of ambient illumination in an almost linear fashion over several orders of magnitude. It may thus transmit information about the daily light-dark cycle to central projection targets in the brain, and exert an important control over putative central oscillators. We have studied single neural elements in the explanted pineal organ of the rainbow trout by combining intracellular recording with intracellular injections of either the fluorescent dye Lucifer Yellow CH or the electron dense marker horseradish peroxidase. After physiological characterization, dye was injected, and the pineal organs were processed for fluorescence or electron microscopy. Horseradish peroxidase-injected cells were selected with light microscopy, and were serially sectioned for electron microscopy. By examining the entire series of ultrathin sections of several labeled cells the following results were obtained. (1) Intensity-graded hyperpolarization that was elicited by light stimuli of all wavelengths could be either purely monophasic at all light intensities, or monophasic at low and intermediate light intensities but with an initial peak transient at response saturation. These two types of responses could be demonstrated to emanate from photoreceptor cells. (2) In addition, an interneuron that responded to light stimulation with intensity-graded hyperpolarizations that decreased in amplitude at high light intensities was identified by analysis of serial ultrathin sections. This interneuron was situated in close opposition to a photoreceptor-like element and another interneuron, both of which contained transcellularly transferred horseradish peroxidase. Transcellular transfer of horseradish peroxidase was repeatedly observed, although in the majority of cases only single cells were labeled. Intracellular injection of Lucifer Yellow CH consistently revealed dye-coupling between photoreceptors and between (inter)neurons. The numbers of labeled elements varied between two and eight cells, after intracellular injection of one cell. The present results indicate that the net neural output of the pineal organ is the result of a relatively complicated neural circuitry, encompassing different types of photoreceptors, interneurons and projection neurons. Electrical coupling between photoreceptors, between neurons, and between photoreceptors and neurons may provide spatial signal averaging. The very slow photoreceptor responses to photic stimulation may provide temporal signal averaging. These two averaging mechanisms might together minimize responses to rapid spatial and temporal changes in the ambient illumination, and thus minimize fluctuations in the neural output of the pineal organ that would be irrelevant to the monitoring of the circadian changes in the photic environment.

Antibodies against retinal photoreceptor‐specific proteins reveal axonal projections from the photosensory pineal organ in teleosts

With the aid of specific antisera to the retinal proteins S-antigen and alpha-transducin and to the rhodopsin apoprotein opsin, we have labeled various cell populations in the pineal organ, parapineal organ, habenular nucleus, and subcommissural organ in two teleost species: the rainbow trout and the European minnow. Although these proteins are associated with photoreceptor functions, not only photoreceptor cells but also the majority of parenchymal cells in the pineal organ were immunoreactive. Immunoreactive cells with dendrite- and axonlike processes were observed also in the parapineal organ and the habenular nucleus. Furthermore, S-antigen-immunoreactive, long, axonal processes were observed in the pineal organ and could be traced from the pineal organ to the habenular nucleus and to the pretectal area. In the light of recent HRP electron microscopical and immunocytochemical studies we propose (1) that not only the classical pineal photoreceptor cells of poikilothermic vertebrates but also other types of CSF-contacting neurons may be the phylogenetic ancestors of mammalian pinealocytes, and (2) a close interrelationship between the pineal organ and the limbic system, effectuated by the direct projections from pineal photoreceptors/CSF-contacting neurons/pinealocytes to the habenular nucleus, and by displaced "pinealocytelike" elements scattered in the habenular nucleus.

GABA-immunoreactive neurons in the photosensory pineal organ of the rainbow trout: two distinct neuronal populations

The distribution of putative GABA-ergic neurons in the photosensory pineal organ of the rainbow trout was investigated by use of a specific antiserum against gamma-aminobutyric acid (GABA). GABA-immunoreactive (GABA-IR) neurons were located in the rostral portion of the pineal end-vesicle, presumably constituting a population of interneurons. GABA-IR neurons were also found in the pineal stalk. The axons of these neurons were traced along the pineal stalk toward the brain. The terminal areas of these axons could not be established. GABA-IR glial cells were observed in the pineal end-vesicle, but not in the pineal stalk.

Putative cholinergic elements in the photosensory pineal organ and retina of a teleost, Phoxinus phoxinus L. (Cyprinidae)

Putative cholinergic neurons in the photosensory pineal organ of a cyprinid teleost, the European minnow, were studied by use of choline acetyltransferase (ChAT) immunocytochemistry and acetylcholinesterase (AChE) histochemistry. Pinealofugally projecting neurons were visualized using retrograde HRP-filling through their cut axons. For comparison, the distribution of choline acetyltransferase immunoreactivity (ChAT-IR) and AChE-positive elements in the retina was investigated. While the distributional patterns of ChAT-IR and strongly AChE-positive perikarya in the retina are similar and may represent the same neuronal population, ChAT-IR and AChE-positive elements in the pineal organ appear to belong to separate populations. In the retina, small- to medium-sized perikarya in the inner nuclear layer, and small perikarya in the ganglion cell layer are ChAT-IR and AChE positive. The entire inner plexiform layer is AChE positive, while only sublaminae 1, 2 and 4 are ChAT-IR. No indication of cholinergic activity was observed in the optic axon layer. In the pineal organ, ChAT-IR is restricted to small perikarya situated rostrally and dorsally in the pineal end-vesicle. AChE-positive neurons are present throughout the pineal end-vesicle and the pineal stalk. The pineal tract (the pinealofugally projecting axons of intrapineal neurons) is strongly AChE positive, but displays no ChAT-IR. The distribution of pinealofugally projecting neurons, labeled with retrogradely transported HRP, is markedly dissimilar to that of the ChAT-IR elements. It is proposed that the photosensory pineal organ transmits photic information to the brain via a non-cholinergic pathway.(ABSTRACT TRUNCATED AT 250 WORDS)

Substance P-like-immunoreactive neurons in the photosensory pineal organ of the rainbow trout, Salmo gairdneri Richardson (Teleostei)

Restricted numbers of substance P-like-immunoreactive (SPL-IR) neurons were demonstrated in the photosensory pineal organ of the rainbow trout. The small parapineal organ of this teleost species receives a distinct SPL-IR innervation via the habenular nuclei, but displays no intrinsic SPL-IR neurons. Intrapineal SPL-IR neurons were located in the rostral portion of the pineal end-vesicle. Neuronal somata were found in a lateral position with smooth axonal processes extending mediad. Immunoreactive somata and axonal processes were observed intraparenchymally as well as in the pineal lumen. The pattern of immunoreactivity was not changed in excised pineal organs that had been incubated in tissue culture medium in the dark for 18 h. The possibility that the intrapineal SPL-IR neurons are not part of the neural circuitry involved in the transduction of photic information, but may have other functions, is discussed.

Effect of GABA and its antagonists, bicuculline and picrotoxin, on nerve cell discharges of the photosensory pineal organ of the frog, Rana esculenta

The effect of γ-aminobutyric acid (GABA) and its antagonists, bicuculline and picrotoxin, was studied on pineal neurons of the frog, Rana esculenta. The drugs were applied by microiontophoresis while monitoring the spontaneous activity and light-evoked responses of electrophysiologically identified achromatic (luminance) neurons of the pineal organ. Almost all neurons investigated were sensitive to GABA. The inhibitory action was characterized by its rapid onset and its reversibility. The GABA antagonists, bicuculline and picrotoxin, were able to antagonize the inhibitory action of the amino acid. The light-evoked inhibition of the maintained ganglion cell activity interfered with the GABA-induced inhibition, i.e. light reduced the strength of inhibition and shortened the effect of GABA. The investigation suggests a major role of GABAergic mechanisms in the ganglion cell output of pineal neurons.

Electrophysiological studies on neuronal transmission in the frog's photosensory pineal organ: The effect of amino acids and biogenic amines

A variety of putative neurotransmitter substances and their analogues were used to characterize the synaptic connections from photoreceptors to ganglion cells in the pineal organ of the frog. The effects of all agents were tested on electrophysiologically identified luminance cells of the pineal organ. l-Aspartate and l-glutamate caused a significant increase of neuronal cell firing, the effects were dose-related, reversible and reproducible. The aspartate and glutamate agonists N-methyl- d-aspartate and kainate possess a similar ability to induce neuronal excitations in the pineal organ, N-methyl- d-aspartate being more potent than kainic acid. The excitatory action of all agents persisted if the ganglion cells were isolated from other synaptic inputs by Co 2+ treatment. The excitatory action of the amino acids was antagonized by d-α-aminoadipate ( d-α-AA); the order of sensitivity to antagonism by d-α-AA was: N-methyl- d-aspartate l-aspartate > l-glutamate ≊ kainate. Taurine, by far the most abundant amino acid in pineal tissues, markedly decreased the spontaneous activity in half of the neurons tested, the remaining cells being unresponsive. The indoleamine serotonin effectively depressed the maintained activity also in half of the cells tested. Acetylcholine had only small effects on pineal luminance cells. It is concluded that l-aspartate (and/or glutamate) might interact with postsynaptic receptors in the ganglion cell membrane and mimics the action of the natural photoreceptor transmitter.

Anatomical and physiological characteristics of pineal photoreceptor cell in the larval lamprey, Petromyzon marinus.

Anatomical and physiological characteristics of pineal photoreceptor cell in the larval lamprey, Petromyzon marinus.G A Pu, and J E DowlingG A Pu, and J E DowlingPublished Online:01 Nov 1981https://doi.org/10.1152/jn.1981.46.5.1018MoreSectionsPDF (4 MB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformation Cited ByThe stepwise development of the lamprey visual system and its evolutionary implications28 February 2018 | Biological Reviews, Vol. 93, No. 3A Cambrian origin for vertebrate rods22 June 2015 | eLife, Vol. 4Nonlinear partial differential equations and applications: Pineal expression-promoting element (PIPE), a cis-acting element, directs pineal-specific gene expression in zebrafish18 November 2002 | Proceedings of the National Academy of Sciences, Vol. 99, No. 24Non-rod, non-cone photoreception in the vertebratesProgress in Retinal and Eye Research, Vol. 21, No. 6Cyclic Nucleotide-Gated Ion ChannelsU. Benjamin Kaupp, and Reinhard Seifert7 January 2002 | Physiological Reviews, Vol. 82, No. 3Signal transmission in the photosensitive pineal organ of the rainbow trout: Modulation of ganglion cell activity by intrinsic dopamineNeurochemistry International, Vol. 27, No. 6Localization of iodopsin and rod-opsin immunoreactivity in the retina and pineal complex of the river lamprey, Lampetra japonicaCell and Tissue Research, Vol. 278, No. 1Neural projections of the pineal organ in the larval sea lamprey (Petromyzon marinus L.) revealed by indocarbocyanine dye tracingNeuroscience Letters, Vol. 164, No. 1-2Signal transmission from pineal photoreceptors to luminosity-type ganglion cells in the lamprey, Lampetra japonicaNeuroscience, Vol. 47, No. 1Immunocytochemical localization of serotonin and photoreceptor-specific proteins (rod-opsin, S-antigen) in the pineal complex of the river lamprey, Lampetra japonica, with special reference to photoneuroendocrine cellsCell and Tissue Research, Vol. 262, No. 2Intracellular responses from UV-sensitive cells in the photosensory pineal organBrain Research, Vol. 534, No. 1-2Intracellular staining of physiologically identified photoreceptor cells and hyperpolarizing interneurons in the teleost pineal organNeuroscience, Vol. 25, No. 3Photoreceptor responses to light in the isolated pineal organ of the trout, Salmo gairdneriNeuroscience, Vol. 25, No. 3External sodium ions are required for the light response in pineal photoreceptorsVision Research, Vol. 28, No. 2Substance P-like-immunoreactive neurons in the photosensory pineal organ of the rainbow trout, Salmo gairdneri Richardson (Teleostei)Cell and Tissue Research, Vol. 246, No. 2Neural response mechanisms in the photoreceptive pineal organ of goldfishComparative Biochemistry and Physiology Part A: Physiology, Vol. 84, No. 3Chromophores in the extraretinal photoreceptor (pineal organ) of teleostsBrain Research, Vol. 338, No. 1Intracellular response and input resistance change of pineal photoreceptors and ganglion cellsNeuroscience Research Supplements, Vol. 2Electrophysiological studies on neuronal transmission in the frog's photosensory pineal organVision Research, Vol. 24, No. 12 More from this issue > Volume 46Issue 5November 1981Pages 1018-38 https://doi.org/10.1152/jn.1981.46.5.1018PubMed7299444History Published online 1 November 1981 Published in print 1 November 1981 Metrics