Does the avian ophthalmic nerve carry magnetic navigational information?

The bobolink (Dolichonyx oryzivorus) uses the earth's magnetic field as one source of directional information for its migratory orientation. However, the location and structure of the magnetoreceptors that transduce the magnetic information to the nervous system are unknown. Because treatment with a strong magnetic pulse results in a change in the direction of orientation, one of the receptors is thought to involve a magnetizable material such as magnetite. The effects of the magnetizing treatment can be abolished (i.e. the bird returns to its original orientation) by blocking the ophthalmic branch of the trigeminal nerve, but the ability of the bird to select and maintain a direction is not affected. These results are consistent with the hypothesis that a magnetizable material such as magnetite is part of the magnetoreceptors that are associated with the ophthalmic nerve.

Effects of light or different earth-strength magnetic fields on the nocturnal melatonin concentration in a migratory bird.

The effects of light or artificial earth-strength magnetic fields (MFs) on pineal melatonin synthesis were studied in the Pied Flycatcher, a migratory bird. Serum melatonin levels exhibited a circadian rhythm with the highest values during the night and lowest during the day. Nocturnal melatonin synthesis was significantly diminished following exposure to light during the night. It was reduced by a similar extend after exposure to an artificial MF that simultaneously reversed the horizontal component of the field and altered its intensity. In contrast, melatonin levels were not significantly changed when the bird was exposed to a MF that changed only in intensity or direction.

MELATONIN IS CRUCIAL FOR THE MIGRATORY ORIENTATION OF PIED FLYCATCHERS (FICEDULA HYPOLEUCA PALLAS)

After pinealectomy, young pied flycatchers tested in the geomagnetic field have been found to be disoriented. In order to examine the possible role of the pineal hormone melatonin, handraised flycatchers were pinealectomized (PX) at the age of 8 weeks. From the day of operation onward, the PXMEL group received 100 µg of melatonin every evening 1 h before darkness, the PXSOL group was injected with the solvent only, and the PX group was untreated. Unoperated birds served as controls. During the following autumn migration, the birds were tested for directional preference in the local geomagnetic field, in the absence of visual cues. The controls were oriented in the species-specific southwesterly direction; pinealectomized birds without additional melatonin (PXSOL, PX) did not show directional preferences. The PXMEL birds that had received daily injections of melatonin also showed significant southwesterly tendencies; their orientation did not differ from that of the controls. This indicates that melatonin is involved in migratory orientation, either in the processes of expressing the genetically encoded information on the migratory course as a direction with respect to the geomagnetic field or in the time programme controlling the specific migratory direction at a given time.

Neuroethological aspects of avian orientation.

Sensory information, which may be essential for the complex process of orientation of birds, is described in this article. The use of vibrational, visual, chemical, olfactory, magnetic cues and their receptive mechanisms, as far as they are known, are explained. Special reference is given to the behavioral and physiological aspects of magnetic sensitivity.

Responses to small magnetic variations by the trigeminal system of the bobolink.

Electrophysiological recordings from the ophthalmic nerve and the trigeminal ganglion of the bobolink (Dolichonyx oryzivorus) indicate the presence of units (14% of the spontaneously active cells) that are sensitive to small changes in the magnetic field. The most common response was an increase in the rate of spontaneous activity. The most sensitive units responded to changes of 200 nT (less than 0.5% of the earth's total field). Other responses included reaction to a 0.5 Hz sinusoidal variation of the magnetic field, and to the movement of a hand-held bar magnet. Because of their sensitivities, the responses to small variations in the magnetic field may be involved in detection of the proposed magnetic navigation map. One possible transducer substance that could account for such a sensitivity is magnetite, which has been previously reported in the upper beak area of the bobolink.

Sensory basis of bird orientation.

Sensory information which may be essential for the complex process of orientation of birds is described in this article. The use of vibrational, visual, chemical, olfactory, magnetic cues and their receptive mechanisms, as far as they are known, are explained. Special reference is given to the behavioral and physiological aspects of magnetic sensitivity.

Pattern of brain glucose utilization following magnetic stimulation.

The 2-deoxy-D-(14C) glucose technique was used for autoradiographic mapping of the local cerebral glucose utilization in pigeons which were exposed to a periodically inverted artificial magnetic field in the Earth's field range. Stimulation during daytime resulted in increased values particularly in primary or secondary visual structures. Stimulation during nighttime resulted in increased values in the optic tectum and within the nucleus isthmi. In both situations decreased values were determined in the hypothalamus and increased values in the pineal gland. The results support the concept that magnetic information is transduced by magnetoreceptors and is relayed to structures of the visual system. Moreover, it is suggested, that magnetic stimulation exerts suppressive metabolic effects on the basal hypothalamus.

Geomagnetic field detection in rodents.

In addition to behavioral evidence for the detection of "earth-strength" magnetic fields (MF) by rodents, recent investigations have revealed that electrophysiological and biochemical responses to MF occur in the pineal organ and retina of rodents. In addition, ferrimagnetic deposits have been identified in the ethmoidal regions of the rodent skull. These findings point to a new sensory phenomenon, which interfaces with many fields of biology, including neuroscience, psychophysics, behavioral ecology, chronobiology and sensory physiology.

Magnetic responses of the trigeminal nerve system of the bobolink (Dolichonyx oryzivorus).

Extracellular recordings using glass microelectrodes were made from the ophthalmic and supraorbital nerves of a transequatorial migratory bird, the bobolink. The rate of electrical activity was modified in 15% of the spontaneously active units by earth-strength alterations of the horizontal or vertical component of the ambient magnetic field using box coils. Responses to magnetic stimulation included augmentation or inhibition of spontaneous activity, or an ON-OFF or OFF response. Responses to magnetic stimulation were also recorded from the optic tectum and the pineal gland. The responses of the trigeminal system are probably independent of the visual system and indicate the presence of two separate magnetic receptor systems in one avian species. The responses from the trigeminal receptor may involve magnetite for transduction of magnetic field information.

Magnetic fields abolish nychthemeral rhythmicity of responses of Purkinje cells to the pineal hormone melatonin in the pigeon's cerebellum.

The effects of micro-electrophoretically applied melatonin on the electrical activity of Purkinje cells in the cerebellum of anaesthetized pigeons were studied. The proportion of excitatory and inhibitory responses to the pineal indoleamine varied significantly depending on whether the cells were tested during the day or at night. This day/night rhythm of responses was abolished if the birds were exposed to complete inversion of the vertical component of an artificial earth's strength magnetic field for one hour at 21.00 h. The results are in line with the concept that pineal involvement in endogenous central nervous rhythms is influenced by changes in the earth's magnetic field.

Neurophysiological properties of magnetic cells in the pigeon's visual system.

Single unit electrical activity was recorded extracellularly in the nucleus of the basal optic root (nBOR) and in the optic tectum under earth-strength magnetic stimulation. Units in the nBOR which were stimulated while the eyes were illuminated by light of different wavelengths exhibited peaks of magnetic responsiveness at 503 nm and 582 nm. Magnetically directional selective cells were found in the stratum griseum et fibrosum superficiale of the optic tectum. They also showed directional selectivity to dynamic photic stimuli. Response peaks varied with the orientation of the pigeon in the horizontal plane. This confirmed that the magnetic responses contained directional information. The results suggest that the receptor and neural organisation of the pigeon's visual system provides an adequate substrate for the detection and elaboration of magnetic compass information.

The avian pineal gland as an independent magnetic sensor.

The electrical activity of pigeon pineal cells was modified by gradual inversion of the natural magnetic field. Effects were also found in blinded birds, and following surgical and chemical interference with the neural connections of the pineal, indicating that the gland possesses intrinsic magnetic sensitivity. The results are in line with the concept that magnetic field detection is associated with photoreceptor activity.

Melatonin lowers excitability of guinea pig hippocampal neurons in vitro.

Action of melatonin (N-acetyl-5-methoxytryptamine; MEL) on guinea pig hippocampal cells (CA3 neurons and dentate granule cells) were studied in vitro using both extra- and intracellular recording. MEL (1-10 mmol/1) had the following effects: Response to repetitive synaptic stimulation was changed drastically: Double shock facilitation (20 ms interval) turned into depression and stimulus trains of a frequency as low as 1 Hz led to a drastic reduction of the response. Membrane potential was hyperpolarized. Duration of action potential was strongly increased. Threshold for the triggering of action potentials was shifted to more positive levels. IPSPs were prolonged and their shunting power enhanced. Repetitive spiking elicited by the application of bicuculline was reversibly abolished. All these effects had in common that cell excitability was lowered. It is concluded that MEL might influence epileptic seizure activity and should be further investigated as potential anticonvulsant.

Changes in the electrical activity of the rat pineal gland following stimulation of the cervical sympathetic ganglia.

In order to elucidate the role of sympathetic innervation for pineal function, the influence of both unilateral and bilateral electrical stimulation of the superior cervical ganglia on the electrical activity of single cells in the rat pineal gland was investigated. These experiments revealed a clear influence on spontaneous electrical activity of single pinealocytes. About half of the units tested by unilateral stimulation exhibited either a graded continuous augmentation or inhibitions of different magnitude. In addition, 'silent' cells without spontaneous activity could be activated by sympathetic stimulation. Sequential and simultaneous bilateral stimulations showed that only a few cells could be influenced by both ganglia and in these cases the influence seemed to be additive. Some pineal cells do not appear to be under the control of the sympathetic nervous system.

Electrical responses of pineal cells to pineal indoles and putative transmitters in intact and blinded pigeons.

The effects of micro-electrophoretically applied pineal indoles, melatonin (MEL), 5-methoxytryptophol (MTL) and 5-hydroxytryptophol (HTL) and of the neurotransmitters, noradrenaline (NOR), acetylcholine (ACH) and gamma-aminobutyric acid (GABA) on the electrical activity of pineal cells were studied in anaesthetized pigeons. Recordings were made from both sighted and blinded birds during both the day- and night-time. Both excitatory and inhibitory responses to the application of all substances tested were observed, while in all cases unresponsive cells were also found. The pattern of responses to MEL, MTL and to NOR varied significantly depending on whether the cells in the sighted pigeons were tested during the day or at night. This day/night rhythm of responses to MEL and to MTL also occurred in the blinded pigeons, although this was not the case for the effects of NOR. Units which were orthodromically excited by electrical stimulation of the habenular complex were also excited by application of GABA. The activity of these units was also likely to be enhanced by application of ACH. The results suggest that the pigeon pineal organ exhibits intrinsic circadian rhythmicity which does not require entrainment signals from the retina. They also indicate that the activity of pineal cells could be influenced by neurotransmitter input provided from within the gland or via its innervation.

Electrophysiological evidence for central nervous connections of the pigeon's pineal gland.

In the pigeon, Columba livia, single unit electrical activity was recorded from 110 cells in the pineal gland. All the cells were classified according to their responses to single shock stimulation of the habenular nuclei and, of these units, 42 cells were subsequently classified according to their response following stimulation of the optic chiasma. Cells were either activated, inhibited or unaffected by the stimulus. No antidromic responses to the stimulation of either site were observed. Habenula stimulation orthodromically induced both excitatory (50% of the cells) and inhibitory (15%) responses. Approximately half the cells tested were unresponsive to stimulation of the optic chiasma, the responding units all being orthodromically excited. No evidence was found for a relationship between the pattern of response to stimulation at the two sites. The results confirm the presence of a central innervation of the pineal in pigeons but suggest that the two pathways are unlikely to converge and the majority of pineal cells do not receive inputs from both of the routes.

Electrophysiological investigations on the central innervation of the rat and guinea-pig pineal gland.

The possible influence of central nervous structures on the electrical activity of single pineal cells was investigated in rat and guinea-pig. In the rat electrical stimulation of the hippocampal formation elicited both single cell responses with different latencies and mostly long-term excitations in single pineal cells, while stimulation of the habenular nuclei caused clear orthodromical responses with different latencies, alterations in the rate of spontaneous electrical activity and evoked discharges of "silent" units. In the guinea-pig electrical stimulation of the paraventricular nucleus influenced predominantly cells in the deeper layers of the posterior part of the pineal gland. Electrical stimulation of both the superior and inferior colliculi elicited field potentials with a constant latency, indicating a functional relationship between the corpora quadrigemina and the pineal organ.

Electrophysiology of the pigeon's habenular nuclei: evidence for pineal connections and input from the visual system.

Single unit electrical activity was recorded from neurons in the habenular nuclei of pigeons. The neurons were initially classified according to their responses to single shock stimulation of the pineal organ and subsequently according to their response following stimulation of the optic chiasma. The cells were also tested for changes in the level of spontaneous activity in response to illumination of the lateral eyes and the exposed dorsal surface of the brain. In response to electrical stimulation at the two sites, cells were either orthodromically activated or inhibited or unaffected by the stimulus. No antidromic responses to stimulation of either site were observed. The results show that habenular neurons receive excitatory and inhibitory afferent fibres from both regions. Evidence is provided for a substantial convergence of either excitatory or inhibitory inputs onto many of these cells. Both excitatory and inhibitory responses to photic stimulation were observed, although almost half of the neurons were unresponsive. No significant relationships were found between response combinations to electrical stimulation at either site and the effects of illumination. This suggests that neither of the afferent pathways demonstrated are primarily concerned with the transfer of photic information.