Firing properties of chopper and delay neurons in the lateral superior olive of the rat

Abstract

Neurons in the lateral superior olivary nucleus (LSO) respond to acoustic stimuli with the "chopper response", a regular repetitive firing pattern with a short and precise latency. In the past, this pattern has been attributed to dendritic integration of synaptic inputs. We investigated a possible contribution of intrinsic membrane properties using intracellular recording techniques in a tissue slice preparation. We found two electrophysiological classes of neurons in the LSO. Chopper neurons responded to depolarizing current pulses with a single onset spike at short, precise latency close to threshold and with repetitive, regular, but accommodating discharges at greater current intensities. An emphasis of response onset and subsequent rate accommodation resulted from the activation of a voltage- and time-dependent sustained outward rectification in a range depolarized from rest. Responses to hyperpolarizing pulses were characterized by an inward rectification, which caused a depolarizing voltage sag in a range negative to -65 mV. Peristimulus time histograms were multimodal, and discharge regularity was evident in narrow unimodal interspike interval time histograms and low coefficients of variation. The accommodation time course was usually fit best by two exponentials with time constants of tau1=3-8 ms and tau2=32-97 ms. Delay neurons responded with a regular repetitive firing to depolarization by current pulses. However, repetitive spike discharge occurred with a prolonged, variable delay of 25-180 ms. High current intensities evoked an additional onset spike with short, precise latency. Activation of a transient outward conductance in the depolarized voltage range caused an early repolarization, which terminated as a depolarizing ramp, reaching spike threshold after the delay. Flat peristimulus time histograms characterized the repetitive discharge in spite of narrow unimodal interspike interval time histograms and low coefficients of variation. Intracellular neurobiotin injections revealed morphological differences between these classes. Chopper neurons were large and fusiform, with a bipolar dendritic distribution oriented perpendicular to the curvature of the LSO. Delay neurons were small and spherical, with highly branched tortuous dendritic arbours of bipolar origin and variable orientation. Chopper and delay neurons are probably LSO principal cells and lateral olivocochlear efferent neurons, respectively. Our findings suggest that the pattern of firing activity of LSO neurons to sound, in vivo, is determined to a large extent by intrinsic membrane properties. Somato-dendritic integration of synaptic inputs are fundamental to the encoding of interaural sound differences, but membrane non-linearities play an important role in determining postsynaptic response patterns.

A Modeling Study of the Effects of Membrane Afterhyperpolarization on Spike Interval Statistics and on ILD Encoding in the Lateral Superior Olive

“…2 and 4 in Tsuchitani and Johnson 1985). Similar tight distributions of first-spike latency have also been reported from in vitro data (Adam et al 1999), despite twofold differences in input resistance between single-spiking and multiple-spiking LSO neurons (Barnes-Davies et al 2004). These results suggest that the repolarization process, but not the cellular mechanisms that give rise to the precise first spike latency, differentiates fast and slow choppers in the LSO.…”

“…The typical modeling assumption that LSO membranes are identical from cell to cell is challenged by physiological studies of ionic channel properties in the LSO (Adam et al 1999;Barnes-Davies et al 2004). Notably, Barnes-Davies et al (2004) show that the expression of potassium channels of the Kv family follows a tonotopic gradient of distributions along the medial-lateral axis in the LSO of young rat, suggesting that membrane excitability of LSO neurons may be differentially modulated by the activity of ionic channels.…”

“…In vitro studies have provided evidence supporting to some extent the heterogeneous onset patterns among LSO neurons. When stimulated with constant step currents, the putative principal LSO neurons respond with either single or repetitive firing patterns (Adam et al 1999(Adam et al , 2001Barnes-Davies et al 2004;Sanes 1990). These in vitro findings stressed that the nonlinear membrane characteristics may give rise to such in vivo like chopping patterns, in contrast to the linear synaptic integration mechanism proposed for the chopper neurons in the ventral cochlear nucleus (Banks and Sachs 1991).…”

Serotonin Shifts First-Spike Latencies of Inferior Colliculus Neurons

“…Serotonin advanced the spikes to an earlier time point, with a slight increase in the spike count, but no change in the interspike interval or first-spike variance. This selective change is consistent with serotonin either decreasing an early inhibitory input that influences latency in many IC neurons (Covey et al, 1996;Oswald et al, 1999;Galazyuk and Feng, 2001;Galazyuk et al, 2005) or decreasing an early transient A-type current that determines latency in other auditory nuclei (olivocochlear neurons, Fujino et al, 1997;Adam et al, 1999; dorsal cochlear nucleus pyramidal neurons, Kanold and Manis, 1999) and is a serotonergic target in Purkinje cells (Wang et al, 1992).…”

Spike-Time Precision and Network Synchrony Are Controlled by the Homeostatic Regulation of the D-Type Potassium Current

“…The control of network synchrony by I D could also be of general importance in other brain regions where the ramp-and-delay phenotype is expressed in principal neurons (Adam et al, 1999;Martina et al, 1999;Russier et al, 2003) or interneurons (Goldberg et al, 2008).…”