In the lateral superior olive (LSO) the firing rate of principal neurons is a linear function of inter-aural sound intensity difference (IID). The linearity and regularity of the "chopper response" of these neurons have been interpreted as a result of an integration of excitatory ipsilateral and inhibitory contralateral inputs by passive soma-dendritic cable properties. To account for temporal properties of this output, we searched for active time- and voltage-dependent nonlinearities in whole cell recordings from a slice preparation of the rat LSO. We found nonlinear current-voltage relations that varied with the membrane holding potential. Repetitive regular firing, supported by voltage oscillations, was evoked by current pulses injected from holding potentials near rest, but the response was reduced to an onset spike of fixed short latency when the pulse was injected from de- or hyperpolarized holding potentials. The onset spike was triggered by a depolarizing transient potential that was supported by T-type Ca(2+)-, subthreshold Na(+)-, and hyperpolarization-activated (I(H)) conductances sensitive, respectively, to blockade with Ni2+, tetrodotoxin (TTX), and Cs+. In the hyperpolarized voltage range, the I(H), was largely masked by an inwardly rectifying K+ conductance (I(KIR)) sensitive to blockade with 200 microM Ba2+. In the depolarized range, a variety of K+ conductances, including A-currents sensitive to blockade with 4-aminopyridine (4-AP) and additional tetraethylammonium (TEA)-sensitive currents, terminated the transient potential and firing of action potentials, supporting a strong spike-rate adaptation. The "chopper response," a hallmark of LSO principal neuron firing, may depend on the voltage- and time-dependent nonlinearities. These active membrane properties endow the LSO principal neurons with an adaptability that may maintain a stable code for sound direction under changing conditions, for example after partial cochlear hearing loss.
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.
The temporal dependence of neuronal responses in the superior olivary complex (SOC) and central nucleus of the inferior colliculus (ICC) were examined using modified forward masking paradigms. Masking and probe tones were at the unit's best frequency and at the same intensity (20-30 dB above threshold). Short-term adaptation was observed in 85 of 113 SOC and in 32 of 50 ICC neurons, and resulted in an average decrease of probe responses (1 or 2 ms after the masker) of 56.3% in SOC neurons and 83.1% in ICC neurons. Recovery from adaptation followed exponential trends, with mean time constants of 106.1 ms and 226.9 ms for SOC and ICC neurons, respectively. Adaptation of inhibition was observed in the lateral superior olive, and may also affect many of the neurons studied. Other ICC neurons (n = 7) exhibited facilitation of probe tone responses, while 6 ICC neurons exhibited more complex temporal changes in responsiveness following a masker.
The hallmark of auditory function in aging adults is difficulty listening in a background of competing talkers, even when hearing sensitivity in quiet is good. Age-related physiological changes may contribute by introducing small timing errors (jitter) to the neural representation of sound, compromising the fidelity of the signal’s fine temporal structure. This may preclude the association of spectral features to form an accurate percept of one complex stimulus, distinct from competing sounds. For simple voiced speech (vowels), the separation of two competing stimuli can be achieved on the basis of their respective harmonic (temporal) structures. Fundamental frequency (F0) differences in competing stimuli facilitate their segregation. This benefit was hypothesized to rely on the adequate temporal representation of the speech signal(s). Auditory aging was simulated via the desynchronization (∼0.25-ms jitter) of the spectral bands of synthesized vowels. The perceptual benefit of F0 difference for the identification of concurrent vowel pairs was examined for intact and jittered vowels in young adults with normal hearing thresholds. Results suggest a role for reduced signal fidelity in the perceptual difficulties encountered in noisy everyday environments by aging listeners. [Work generously supported by the Michael Smith Foundation for Health Research.]
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