A dendritic model of coincidence detection in the avian brainstem

Biological Cybernetics, 2003

A biologically detailed model of the binaural avian nucleus laminaris is constructed, as a twodimensional array of multicompartment, conductance-based neurons, along tonotopic and interaural time delay (ITD) axes. The model is based primarily on data from chick nucleus laminaris. Typical chick-like parameters perform ITD discrimination up to 2 kHz, and enhancements for barn owl perform ITD discrimination up to 6 kHz. The dendritic length gradient of NL is explained concisely. The response to binaural out-of-phase input is suppressed well below the response to monaural input (without any spontaneous activity on the opposite side), implicating active potassium channels as crucial to good ITD discrimination.

Frontiers in Computational Neuroscience, 2013

Interaural time difference (ITD), or the difference in timing of a sound wave arriving at the two ears, is a fundamental cue for sound localization. A wide variety of animals have specialized neural circuits dedicated to the computation of ITDs. In the avian auditory brainstem, ITDs are encoded as the spike rates in the coincidence detector neurons of the nucleus laminaris (NL). NL neurons compare the binaural phase-locked inputs from the axons of ipsi-and contralateral nucleus magnocellularis (NM) neurons. Intracellular recordings from the barn owl's NL in vivo showed that tonal stimuli induce oscillations in the membrane potential. Since this oscillatory potential resembled the stimulus sound waveform, it was named the sound analog potential (Funabiki et al., 2011). Previous modeling studies suggested that a convergence of phase-locked spikes from NM leads to an oscillatory membrane potential in NL, but how presynaptic, synaptic, and postsynaptic factors affect the formation of the sound analog potential remains to be investigated. In the accompanying paper, we derive analytical relations between these parameters and the signal and noise components of the oscillation. In this paper, we focus on the effects of the number of presynaptic NM fibers, the mean firing rate of these fibers, their average degree of phase-locking, and the synaptic time scale. Theoretical analyses and numerical simulations show that, provided the total synaptic input is kept constant, changes in the number and spike rate of NM fibers alter the ITD-independent noise whereas the degree of phase-locking is linearly converted to the ITD-dependent signal component of the sound analog potential. The synaptic time constant affects the signal more prominently than the noise, making faster synaptic input more suitable for effective ITD computation.

Frontiers in Computational Neuroscience, 2013

A wide variety of neurons encode temporal information via phase-locked spikes. In the avian auditory brainstem, neurons in the cochlear nucleus magnocellularis (NM) send phase-locked synaptic inputs to coincidence detector neurons in the nucleus laminaris (NL) that mediate sound localization. Previous modeling studies suggested that converging phase-locked synaptic inputs may give rise to a periodic oscillation in the membrane potential of their target neuron. Recent physiological recordings in vivo revealed that owl NL neurons changed their spike rates almost linearly with the amplitude of this oscillatory potential. The oscillatory potential was termed the sound analog potential, because of its resemblance to the waveform of the stimulus tone. The amplitude of the sound analog potential recorded in NL varied systematically with the interaural time difference (ITD), which is one of the most important cues for sound localization. In order to investigate the mechanisms underlying ITD computation in the NM-NL circuit, we provide detailed theoretical descriptions of how phase-locked inputs form oscillating membrane potentials. We derive analytical expressions that relate presynaptic, synaptic, and postsynaptic factors to the signal and noise components of the oscillation in both the synaptic conductance and the membrane potential. Numerical simulations demonstrate the validity of the theoretical formulations for the entire frequency ranges tested (1-8 kHz) and potential effects of higher harmonics on NL neurons with low best frequencies (<2 kHz).

The Journal of the Acoustical Society of America, 2009

In the mammalian auditory brainstem, two types of coincidence detector cells are involved in binaural localization: excitatory-excitatory ͑EE͒ and excitatory-inhibitory ͑EI͒. Using statistics derived from EE and EI spike trains, binaural discrimination abilities of single tones were predicted. The minimum audible angle ͑MAA͒, as well as the just noticeable difference of interaural time delay ͑ITD͒ and interaural level difference ͑ILD͒ were analytically derived for both EE and EI cells on the basis of two possible neural coding patterns, rate coding that ignores a spike's timing information and all-information coding ͑AIN͒, which considers a spike's timing occurrences. Simulation results for levels below saturation were qualitatively compared to experimental data, which yielded the following conclusions: ͑1͒ ITD is primarily estimated by EE cells with AIN coding when the ipsilateral auditory input exhibits phase delay between 40°and 65°. ͑2͒ In ILD, both AIN and rate coding provide identical performances. It is most likely that ILD is primarily estimated by EI cells according to rate coding, and for ILD the information derived from the spikes' timing is redundant. ͑3͒ For MAA estimation, the derivation should take into account ambiguous directions of a source signal in addition to its true value.

The Journal of Neuroscience

Neurons of the owl's nucleus laminaris serve as coincidence detectors for measurement of interaural time difference. The discharge rate of nucleus laminaris neurons for both monaural and binaural stimulation increased with sound intensity until they reached an asymptote. Intense sounds affected neither the ratio between binaural and monaural responses nor the interaural time difference for which nucleus laminaris neurons were selective. Theoretical analysis showed that high afferent discharge rates cause coincidence detectors with only excitatory input to lose their selectivity for interaural time difference when coincidence of impulses from the same side becomes as likely as that of impulses from the two sides. We hypothesize that inhibitory input whose strength increases with sound intensity protects nucleus laminaris neurons from losing their sensitivity to interaural time difference with intense sounds.

Nature Neuroscience, 2010

Neurons in the medial superior olive process sound-localization cues via binaural coincidence detection, in which excitatory synaptic inputs from each ear are segregated onto different branches of a bipolar dendritic structure and summed at the soma and axon with submillisecond time resolution. Although synaptic timing and dynamics critically shape this computation, synaptic interactions with intrinsic ion channels have received less attention. Using paired somatic and dendritic patch-clamp recordings in gerbil brainstem slices together with compartmental modeling, we found that activation of K v 1 channels by dendritic excitatory postsynaptic potentials (EPSPs) accelerated membrane repolarization in a voltage-dependent manner and actively improved the time resolution of synaptic integration. We found that a somatically biased gradient of K v 1 channels underlies the degree of compensation for passive cable filtering during propagation of EPSPs in dendrites. Thus, both the spatial distribution and properties of K v 1 channels are important for preserving binaural synaptic timing.

Neurocomputing, 2003

Neuronal activity of cells in the ÿrst binaural brainstem nucleus, in mammals the MSO, depends on interaural time di erences (ITDs). The neurons thereby resolve disparities of about 10 s. Based on a computational model for the development of synaptic couplings, we give restrictions for a recently proposed coding hypothesis based on a monotonic dependence of the ÿring rate upon the ITD. We ÿnd that synaptic plasticity at MSO neurons with high best frequencies favors a rate-place code with a high variability of the tuning curves, as in the classical Je ress model, whereas low best frequencies give rise to monotonic ITD dependence.

Nature Communications, 2014

Neurons in the medial superior olive (MSO) detect microsecond differences in the arrival time of sounds between the ears (interaural time differences or ITDs), a crucial binaural cue for sound localization. Synaptic inhibition has been implicated in tuning ITD sensitivity, but the cellular mechanisms underlying its influence on coincidence detection are debated. Here we determine the impact of inhibition on coincidence detection in adult Mongolian gerbil MSO brain slices by testing precise temporal integration of measured synaptic responses using conductance-clamp. We find that inhibition dynamically shifts the peak timing of excitation, depending on its relative arrival time, which in turn modulates the timing of best coincidence detection. Inhibitory control of coincidence detection timing is consistent with the diversity of ITD functions observed in vivo and is robust under physiologically relevant conditions. Our results provide strong evidence that temporal interactions between excitation and inhibition on microsecond timescales are critical for binaural processing. synaptically evoked (blue) and conductance-clamp-simulated (black) EPSPs. Negative and positive values indicate an EPSP peak advance and delay, respectively. Dt inh ¼ 0.1 ms, P ¼ 0.986; Dt inh ¼ À 0.6 ms, P ¼ 0.647; two-way ANOVA, n ¼ 7 recordings.

Journal of Neurophysiology, 2012

Owls use interaural time differences (ITDs) to locate a sound source. They compute ITD in a specialized neural circuit that consists of axonal delay lines from the cochlear nucleus magnocellularis (NM) and coincidence detectors in the nucleus laminaris (NL). Recent physiological recordings have shown that tonal stimuli induce oscillatory membrane potentials in NL neurons (Funabiki K, Ashida G, Konishi M. J Neurosci 31: 15245–15256, 2011). The amplitude of these oscillations varies with ITD and is strongly correlated to the firing rate. The oscillation, termed the sound analog potential, has the same frequency as the stimulus tone and is presumed to originate from phase-locked synaptic inputs from NM fibers. To investigate how these oscillatory membrane potentials are generated, we applied recently developed signal-to-noise ratio (SNR) analysis techniques (Kuokkanen PT, Wagner H, Ashida G, Carr CE, Kempter R. J Neurophysiol 104: 2274–2290, 2010) to the intracellular waveforms obtaine...

Neurocomputing, 2001

An orderly spatial representation of the azimuthal position of a sound source has been observed in many animals. Barn owls, e.g., derive the azimuth from a neuronal map of interaural time di!erences (ITD) with a temporal precision of a few microseconds. We present a model of how an ITD map can develop in an array of spiking neurons in the barn owl's nucleus laminaris. We have combined homosynaptic spike-based Hebbian learning with presynaptic propagation of synaptic modi"cations. The latter is a feasible interaction mechanism between neurons and may be orders of magnitude weaker than the former. It is a key to explaining the widely assumed place code proposed by Je!ress (J. Comput. Physiol. Psychol. 41 (1948) 35).