Synaptic inhibition influences the temporal coding properties of medial superior olivary neurons: An in vitro study

The medial superior olive (MSO) functions as a coincidence detector for interaural time and phase differences by integrating excitatory synaptic inputs. Recent studies demonstrating glycinergic projections to MSO neurons suggest that coincidence detection results from the temporal integration of both EPSPs and IPSPs. We examined the impact of synaptic inhibition on the temporal coding properties of gerbil MSO neurons in vitro with intracellular recordings and electrical stimulation. For low-level bilateral electric stimulation, the EPSPs summated to produce an action potential in 73% of MSO neurons if they occurred within 50-500 μsec of one another. Synaptic inhibition became more prominent at higher stimulus amplitudes in 73% of MSO neurons, and could block an evoked action potential if the stimuli to each pathway were delivered within 250 μsec of one another. The glycine receptor antagonist strychnine influenced the response to simulated interaural time differences. In the presence of strychnine, interstimulus delays that originally resulted in full action potential suppression were sufficient to evoke an action potential. For trains of stimuli, as stimulus intensity increased (spatial summation), or as stimulus repetition rate increased to 100-500 Hz (temporal summation), there was a decrease in the number of stimulus pulses that evoked an action potential. In the presence of strychnine, MSO neurons generated a greater percentage of action potentials to the stimulus trains. When stimulus trains were delivered bilaterally, MSO neurons fired a greater number of action potentials at specific interstimulus time differences, and were selectively inhibited at other time differences. We conclude that time-specific response characteristics of MSO neurons are governed not only by the coincidence of synaptic excitation, but also by the coincidence and temporal summation of synaptic inhibition. This should enable MSO neurons to respond selectively not only to interaural time differences, but also to sounds with complex time patterns.