Adaptation in the inferior colliculus of the barn owl (Tyto alba) as demonstrated by a two-stimulus paradigm

Martin Singheiser

RWTH Aachen Universität


Neurons typically respond with a higher rate to the onset of a stimulus than during ongoing stimulation. This decline in their initially high response rate to a steady-state at later phases of the stimulus presentation is termed spike-frequency adaptation. The underlying mechanism is different from adaptation-of-excitation, where the capacity of a neuron to respond to subsequent stimuli is reduced, when the first stimulus was excitatory itself. Adaptation has been observed at almost all levels of the auditory system and is linked with effects like the ''dynamic-range problem'' or novelty detection.

In this study we were interested whether adaptation occurs in monaural responses of the narrowband neurons in the central nucleus of the inferior colliculus (ICC). Working with anaesthetized owls and using standard extracellular recording techniques, we first determined the best frequency (BF) of a neuron. Stimuli were tones of varying frequency with 100 ms duration and 5 ms cosine-squared on and off ramps. Secondly, a monaural rate level function (RLF) was recorded at the BF. We then tested adaptation at BF by presenting two consecutive stimuli. The first stimulus was presented at a given level (10%, 30%, 50%, 70%, 90% of the saturating responses) whereas the second stimulus was presented either at varying inter-stimulus intervals (ISI, ISI tuning, ISI varying from 25 ms to 1600 ms, equal levels) or at varying levels of the second stimulus (level tuning, ISI = 0 ms, level varying in 5 dB steps from 0 to 25 dB louder). The change of the response was measured in two ways. The response ratio is the quotient of the response to the second stimulus divided by the response to the first stimulus multiplied by 100. The adaptation ratio was defined as the percent charge from the maximum peak in the PSTH to the adapted rate of the last ten bins of the stimulus (bin size = 1ms).

In the level tuning, the response to the second stimulus was reduced when both stimuli had the same intensity, irrespective of the level of the saturating response of the monaural RLF. An average increase of +5 dB in signal amplitude caused the response to the second stimulus to increase for levels up to 70% of the saturating response. In the ISI tuning, the neurons showed no reduced response ratio to the second stimulus after an interval of 100-400 ms for contralateral stimulation and about 50 ms for ipsilateral stimulation when both stimuli had the same intensity.

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