GABAergic disinhibition affects responses of bat inferior collicular neurons to temporally patterned sound pulses.
Using the big brown bat, Eptesicus fuscus, as a model mammalian auditory system, we studied the effect of GABAergic disinhibition by bicuculline on the responses of inferior collicular (IC) neurons to temporally patterned trains of sound pulses delivered at different pulse repetition rates (PRRs) under free-field stimulation conditions. All 66 neurons isolated from eight bats either discharged one to two impulses (phasic on responders, n = 41, 62%), three to eight impulses (phasic bursters, n = 19, 29%), or many impulses throughout the entire duration of the stimulus (tonic responders, n = 6, 9%). Whereas 50 neurons responded vigorously to frequency-modulated (FM) pulses, 16 responded poorly or not at all to FM pulses. Bicuculline application increased the number of impulses of all 66 neurons in response to 4 ms pulses by 15-1,425%. The application also changed most phasic on responders into phasic bursters or tonic responders, resulting in 12 (18%) phasic on responders, 34 (52%) phasic bursters, and 20 (30%) tonic responders. Response latencies of these neurons were either shortened (n = 25, 38%) by 0.5-6.0 ms, lengthened (n = 9, 14%) by 0. 5-2.5 ms or not changed (n = 32, 48%) on bicuculline application. Each neuron had a highest response repetition rate beyond which the neuron failed to respond. Bicuculline application increased the highest response repetition rates of 62 (94%) neurons studied. The application also increased the highest 100% pulse-locking repetition rates of 21 (32%) neurons and facilitated 27 (41%) neurons in response to more pulses at the same PRR than predrug conditions. According to average rate-based modulation transfer functions (average rate MTFs), all 66 neurons had low-pass filtering characteristics both before and after bicuculline application. According to total discharge rate-based modulation transfer functions (total rate MTFs), filtering characteristics of these neurons can be described as band-pass (n = 52, 79%), low-pass (n = 12, 18%), or high-pass (n = 2, 3%) before bicuculline application. Bicuculline application changed the filtering characteristics of 14 (21%) neurons. According to synchronization coefficient-based modulation transfer functions, filtering characteristics of these neurons can be described as low-pass (n = 41, 62%), all-pass (n = 11, 17%), band-suppression (n = 7, 10.5%), and band-suppression-band-pass filters (n = 7, 10.5%). Bicuculline application changed filtering characteristics of 19 (29%) neurons.
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Division of Biological Sciences, The University of Missouri, Columbia, Missouri 65211, USA.
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Wu
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D000161:Acoustic Stimulation; D000818:Animals; D001640:Bicuculline / Q000494:pharmacology*; D002685:Chiroptera / Q000502:physiology*; D004455:Echolocation / Q000502:physiology; D018756:GABA Antagonists / Q000494:pharmacology*; D006309:Hearing / Q000502:physiology*; D007245:Inferior Colliculi / Q000187:drug effects* / Q000502:physiology; D009474:Neurons / Q000502:physiology; D010507:Periodicity; D011930:Reaction Time; D005680:gamma-Aminobutyric Acid / Q000502:physiology*
D018756:GABA Antagonists; D005680:gamma-Aminobutyric Acid; D001640:Bicuculline