Shunting Inhibition in Accessory Optic System Neurons

Abstract

. The interaction of excitatory and inhibitory inputs to the accessory optic system was studied with whole cell recordings in the turtle basal optic nucleus. Previous studies have shown that visual patterns, drifting in the same preferred direction, evoke excitatory and inhibitory postsynaptic events simultaneously. Analysis of the reversal potentials for these events and their pharmacological profile suggest that they are mediated by AMPA and GABA A receptors, respectively. Here, neurons were recorded to study nonlinear interaction between excitatory and inhibitory responses evoked by electrical microstimulation of the retina and pretectum, respectively. The responses to coincident activation of excitatory and inhibitory inputs exhibited membrane shunting in that the excitatory response amplitude, adjusted for changes in driving force, was attenuated during the onset of the inhibitory response. This nonlinear interaction was seen in many but not all stimulus pairings. In some cases, attenuation was followed by an augmentation of the excitatory response. For comparison, the size of the excitatory response was evaluated during a hyperpolarizing current pulse that directly modulated voltage-sensitive channels of a slow rectifying I h current. Injection of hyperpolarizing current did not cause the attenuation of the excitatory synaptic responses. We conclude that there is a nonlinear interaction between these excitatory and inhibitory synaptic currents that is not due to hyperpolarization itself, but probably is a result of their own synaptic conductance changes, i.e., shunting. Since these events are evoked by identical visual stimuli, this interaction may play a role in visual processing. I N T R O D U C T I O NNeurons may receive tens of thousands of synaptic inputs that are integrated throughout its membrane, often resulting in spike initiation at the axon hillock near the soma. This synaptic integration occurs during a temporal overlap of synaptic events that involve different synaptic conductances (e.g., excitatory and inhibitory responses; Qian and Sejnowski 1990). The experiments here investigate synaptic integration on a membrane level in a system for which it has been shown that natural stimuli evoke simultaneous excitatory and inhibitory inputs onto the same cell (Ariel and Kogo 2001). These cells in the accessory optic system relay retinal slip information to the cerebellum and numerous brain stem nuclei for compensatory head and eye movements (Brecha and Karten 1979;Simpson 1984).The accessory optic system receives direct excitatory input from the retina (Kogo and Ariel 1997;Zhang and Eldred 1994) and indirect inhibitory input from the pretectum (Kogo et al. 2002). Both excitatory and inhibitory responses to pattern motion on the contralateral retina are direction-sensitive (Ariel and Kogo 2001). Surprisingly, these two inputs shared a similar preferred direction such that excitatory and inhibitory synaptic events reach the membrane simultaneously.To study synaptic integration of these two inputs, mi...

Projections of the nucleus lentiformis mesencephali in pigeons (Columba livia): A comparison of the morphology and distribution of neurons with different efferent projections

“…Electrophysiological studies lend support to the assertion that the nBOR‐projecting LM neurons are, at least in part, GABAergic. In turtles, Ariel and Kogo (2005) noted that the nBOR receives an inhibitory input (“shunting inhibition”) from LM, which is blocked by a GABA A receptor antagonist. Nogueira and Britto (1991) recorded from nBOR neurons in pigeons in response to electrical stimulation of LM.…”