The Journal of Neuroscience, December 15, 2002, 22(24):11004-11018
Interaction of Excitation and Inhibition in Anteroventral
Cochlear Nucleus Neurons That Receive Large Endbulb Synaptic
Endings
Cornelia
Kopp-Scheinpflug1,
Susanne
Dehmel1,
Gerd J.
Dörrscheidt2, and
Rudolf
Rübsamen1
1 Department of Neurobiology, University of Leipzig,
04103 Leipzig, Germany, and 2 Department of General Zoology
and Neurobiology, Ruhr-University Bochum, Bochum, 44801 Germany
Spherical bushy cells (SBCs) of the anteroventral cochlear nucleus
(AVCN) receive their main excitatory input from auditory nerve fibers
(ANFs) through large synapses, endbulbs of Held. These cells are also
the target of inhibitory inputs whose function is not well understood.
The present study examines the role of inhibition in the encoding of
low-frequency sounds in the gerbil's AVCN. The presynaptic action
potentials of endbulb terminals and postsynaptic action potentials of
SBCs were monitored simultaneously in extracellular single-unit
recordings in vivo. An input-output analysis of
presynaptic and postsynaptic activity was performed for both
spontaneous and acoustically driven activity. Two-tone stimulation and
neuropharmacological experiments allowed the effects of neuronal
inhibition and cochlear suppression on SBC activity to be distinguished.
Ninety-one percent of SBCs showed significant neuronal inhibition.
Inhibitory sidebands enclosed the high- or low-frequency, or both,
sides of the excitatory areas of these units; this was reflected as a
presynaptic to postsynaptic increase in frequency selectivity of up to
one octave. Inhibition also affected the level-dependent responses at
the characteristic frequency. Although in all units the presynaptic
recordings showed monotonic rate-level functions, this was the case in
only half of the postsynaptic recordings. In the other half of SBCs,
postsynaptic inhibitory areas overlapped the excitatory areas,
resulting in nonmonotonic rate-level functions. The results demonstrate
that the sound-evoked spike activity of SBCs reflects the integration
of acoustically driven excitatory and inhibitory input. The inhibition
specifically affects the processing of the spectral, temporal, and
intensity cues of acoustic signals.
Key words:
prepotential units; endbulb of Held; cochlear
suppression; neuronal inhibition; in vivo physiology; bicuculline; strychnine; gerbil; spherical bushy cells; cochlear
nucleus
Copyright © 2002 Society for Neuroscience 0270-6474/02/222411004-15$05.00/0
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