Physiological and anatomical characteristics of reticulospinal neurones in lamprey

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Abstract
1. Intracellular records were obtained from giant reticulospinal cells (Müller cells) in the brain of adult lamprey. The cells had maximum resting potentials of -80 mV and action potentials with overshoots of 30 mV. Input resistances varied from 2 to 8 MΩ. 2. Individual spontaneous excitatory and inhibitory synaptic potentials (e.p.s.p.s and i.p.s.p.s) were observed, as well as occasional high frequency bursts of excitatory potentials. Much of the spontaneous synaptic activity could be eliminated by elevating the Ca2+ concentration in the bathing solution to 10-15 m M, suggesting that the synaptic potentials were due to spike activity in elements presynaptic to Müller cells. 3. Electrical stimulation of cranial nerves produced synaptic responses in Müller cells. Ipsilateral vestibular nerve stimulation produced i.p.s.p.s; contralateral stimulation, e.p.s.p.s. Stimulation of either optic nerve produced mixed synaptic responses with e.p.s.p.s dominating in cells with large resting potentials. Trigeminal nerve stimulation produced mixed responses. Olfactory nerve stimulation produced excitation. Spinal cord stimulation produced e.p.s.p.s and i.p.s.p.s, the dominant effect being inhibition. 4. In favourable preparations strong electrical stimulation of cranial nerves produced afterdisharges in Müller cells, lasting from a few seconds after stimulation of the olfactory and vestibular nerves to as long as several minutes after optic, trigeminal or spinal cord stimulation. 5. Natural stimulation of tactile, visual and vestibular receptors resulted in synaptic responses similar to those produced by electrical stimulation of the cranial nerves. Fish odour applied to the olfactory mucosa produced no response. 6. Iontophoretic application of L-glutamate to Müller cells produced depolarization accompanied by a decrease in input resistance. In addition, glutamate produced bursts of inhibitory and excitatory synaptic potentials, presumably by depolarizing excitatory or inhibitory nerve terminals or nearby cell bodies. 7. Iontophoretic application of γ-aminobutyric acid (GABA) resulted in a slight hyperpolarization, accompanied by a large reduction in input resistance. The reversal point both of the hyperpolarizations and of the spontaneous inhibitory post-synaptic potentials was about 6 mV greater than the resting potential. 8. There were two types of synaptic ending on Müller cell bodies, one type containing round vesicles and the other containing ellipsoidal vesicles. These terminals were intermixed over the surface of the cell bodies and dendrites with no readily apparent segregation. 9. Intracellular records from the spinal axons of Müller cells during electrical stimulation of cranial nerves and spinal cord showed, in addition to the normal propagating action potential activity which normally originates in the cell bodies, depolarizing, hyperpolarizing and biphasic evoked potentials. These membrane responses were grossly similar in appearance to synaptic potentials except that the large depolarizing potentials had unusually long decay times. The physiological basis of these potentials remains unclear. 10. Electron microscopic examination showed very few synaptic endings afferent to Müller axons, a finding in contrast to the abundance of synaptic-like potentials recorded. However, the occasional synapses afferent to Müller axons were invariably located near an efferent synaptic region of the axon itself. This raises the possibility that a very limited number of synaptic regions of Müller axons may be subject to presynaptic modulation of transmitter release. 11. The observations reported here support the idea that Müller cells in lamprey are an important motor outflow from the brain and serve to coordinate the lamprey's trunk responses to external sensory stimulation.