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Departments of Pharmacology and Physiology, University of California School of Medicine, San Francisco, CA 94143, U.S.A.
1. Intracellular recordings from an in vitro preparation of turtle olfactory bulb were used to determine the pathway responsible for producing synaptic inhibition of mitral cells.
2. Inhibitory post-synaptic potentials (i.p.s.p.s) could be elicited in mitral cells by both olfactory nerve (orthodromic) and mitral cell axon (antidromic) stimulation and by suprathreshold depolarizing current pulses injected intracellularly through the recording micro-electrode. Reversing the chloride gradient by either intracellular injection of chloride or lowering the external chloride concentration reversed the i.p.s.p.s into depolarizing potentials. The GABA antagonists, bicuculline and picrotoxin, blocked the i.p.s.p.s.
3. A large increment in the size of the orthodromic and antidromic i.p.s.p. was associated with an action potential. Grading the stimulus intensity on either side of threshold resulted in graded changes in the size of the i.p.s.p. The increment associated with an action potential and the ability to evoke an i.p.s.p. by direct stimulation of a mitral cell suggested that these phenomena were due to activation of the dendrodendritic reciprocal synapses between mitral and granule cells.
4. Orthodromic, antidromic and directly produced action potentials could be fractionated such that regenerative activation of the soma-dendritic membrane could be blocked. Only when this membrane was allowed to reach threshold was a large i.p.s.p. recorded. This indicated that the increment in the i.p.s.p. was due to activation of a synaptic pathway involving the soma-dendritic membrane.
5. When spike propagation in the mitral cell axons was blocked by tetrodotoxin (TTX), an i.p.s.p. could still be produced by direct stimulation, indicating that the mitral cell soma-dendritic membrane is functionally both pre- and post-synaptic. TTX blocked the fast, high amplitude somatic spikes and revealed higher threshold, broader spikes of lower amplitude that were blocked by cobalt and calcium-free Ringer.
6. Tetraethylammonium (TEA) increased the duration and the amplitude of the calcium spike. The amplitude was also increased by barium which prolonged the spike only if TEA was present. In the presence of TEA, bicuculline also prolonged the calcium spike. This suggests that three ionic conductances limit the duration of the calcium action potential: a voltage-dependent potassium conductance, a calcium-dependent potassium conductance, and the chloride conductance associated with the i.p.s.p.
7. Spontaneous, bicuculline-sensitive, depolarizing potentials were recorded in mitral cells impaled with KCl-filled electrodes. Orthodromic or antidromic stimulation increased the frequency of these small potentials for the duration of the i.p.s.p., indicating prolonged GABA release.
8. Stimulation of the olfactory nerves, the mitral cell axons, and direct stimulation could elicit action potentials in granule layer cells. Orthodromic and antidromic activation was followed by a hyperpolarization of about the same duration as the mitral cell i.p.s.p. and was probably the result of dysfacilitation.
9. Paired stimulation of the mitral cell axons resulted in the diminution of the granule cell e.p.s.p. evoked by the second shock, indicating that the predominant excitatory input to the granule cells is through the mitral cell dendrites.
10. It is concluded that both synaptic inhibition of mitral cells and excitation of granule cells is mediated primarily by the dendrodendritic reciprocal pathway.
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