Monosynaptic and polysynaptic feed-forward inputs to mitral cells from olfactory sensory neurons

• Published in: The Journal of neuroscience 2011-06, Vol.31 (24), p.8722-8729
• Main Authors: Najac, Marion, De Saint Jan, Didier, Reguero, Leire, Grandes, Pedro, Charpak, Serge
• Format: Article
• Language: English
• Subjects: 2-Amino-5-phosphonovalerate - pharmacology; Action Potentials - physiology; Animals; Animals, Newborn; Biophysics; Chromones - pharmacology; Electric Stimulation; Excitatory Amino Acid Antagonists - pharmacology; Excitatory Postsynaptic Potentials - drug effects; Excitatory Postsynaptic Potentials - physiology; Female; GABA Antagonists - pharmacology; In Vitro Techniques; Life Sciences; Luminescent Proteins - genetics; Male; Mice; Mice, Transgenic; Nerve Net - cytology; Nerve Net - physiology; Neurobiology; Neurons - classification; Neurons - drug effects; Neurons - physiology; Neurons and Cognition; Olfactory Bulb - cytology; Patch-Clamp Techniques; Pyridazines - pharmacology; Synapses - classification; Synapses - drug effects; Synapses - physiology
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/jneurosci.0527-11.2011

Olfactory sensory neurons (OSNs) expressing the same odorant receptor converge in specific glomeruli where they transmit olfactory information to mitral cells. Surprisingly, synaptic mechanisms underlying mitral cell activation are still controversial. Using patch-clamp recordings in mouse olfactory bulb slices, we demonstrate that stimulation of OSNs produces a biphasic postsynaptic excitatory response in mitral cells. The response was initiated by a fast and graded monosynaptic input from OSNs and followed by a slower component of feedforward excitation, involving dendro-dendritic interactions between external tufted, tufted and other mitral cells. The mitral cell response occasionally lacked the fast OSN input when few afferent fibers were stimulated. We also show that OSN stimulation triggers a strong and slow feedforward inhibition that shapes the feedforward excitation but leaves unaffected the monosynaptic component. These results confirm the existence of direct OSN to mitral cells synapses but also emphasize the prominence of intraglomerular feedforward pathways in the mitral cell response.