Intracellular study of auditory coincidence detector neurons in owls

To elucidate the cellular mechanism for detection of interaural time difference (ITD), we recorded intracellularly from the owl’s nucleus laminaris in vivo. Its neurons produced small action potentials and sinusoidal oscillatory postsynaptic potentials whose frequency corresponded to the frequency of stimulus tones. The significance of these phenomena for ITD detection will be discussed. Owls can detect interaural time differences with an accuracy of a few tens of microseconds for sound localization. Nucleus Laminaris (NL) is a 3 order auditory relay station in the brainstem, and its neurons serve as coincidence detectors of binaural signals for the computation of the interaural time difference (ITD). The cellular mechanism for coincidence detection has long been the subject of discussion and modeling. The lines of evidence used in these models came from in vitro intracellular studies of chick’s nucleus laminaris [2,7,8], extracelluar studies of owl’s nucleus laminaris neurons [3], and owl’s behavioral performance [4]. However, the mechanisms that were proposed to explain the processing of ITDs remain untested. Intracellular recordings from owl’s nucleus laminaris in vivo are therefore, necessary. As NL is located in the brainstem, aspiration of the cerebellum is usually necessary to access NL with microelectrodes, which will prevent repetitive use of the same owl for experiments. Brain pulsations that start a couple of hours after aspiration of the cerebellum prevent stable intracellular recording. We, therefore, developed a new technique to overcome the difficulties by using coaxial glass electrodes in which one (microelectrode) was inserted into a patch-electrode type capillary. The tip of the microelectrode was protected by the outer one during penetration. Also, a small amount of oil at the tip of the outer electrode reduced the capacitance of the microelectrode [1]. These two electrodes were advanced by two independent microdrives [5]. We drove both electrodes across the cerebellum to the depth of 7-10 mm where we began to advance the microelectrode into the brainstem. We could perform intracellular recording from neurons located up to 15 mm away from the brain surface with this technique. NL neurons produced small action potentials and sinusoidal oscillatory potentials whose frequency corresponded to the stimulus sound. These sound analogue psps changed their amplitudes with ITD. The number of spikes evoked by sound changed with the amplitude of the sound analogue psps. The owl’s NL neuron is supposed to receive convergent inputs from about 45-100 magnocellularis (NM) neurons of each side [10], and NM neurons phaselock [11]. The sound analogue psps can be generated by the convergence of phase locked inputs. However there are several conditions that must be considered. First, NM neurons’ phase locking is not perfect especially at higher frequencies [11]. There should be a considerable amount of phase jitter, which will affect the formation of sound analogue potentials. Second, although extraordinarily fast epscs were reported in chick NM [12] and NL [7] neurons in vitro, it is still not fast enough to avoid temporal summation above 4kHz. These and other important problems await future investigations. Small spikes were also reported in other auditory neurons, for example, octopus cells in mammalian cochlear nucleus, which are supposed to serve for detection of coincident firing of auditory nerve fibers [9]. Carr et al [6] reported that the initial