HIGH-FREQUENCY NEURONS IN THE INFERIOR COLLICULUS THAT ARE SENSITIVE TO INTERAURAL DELAYS OF AMPLITUDE-MODULATED TONES - EVIDENCE FOR DUAL BINAURAL INFLUENCES

1. Localization of sounds has traditionally been considered to be performed by a duplex mechanism utilizing interaural temporal differences (ITDs) at low frequencies and interaural intensity differences at higher frequencies. More recently, it has been found that listeners can detect ITDs at high frequencies if the amplitude of the sound varies and an ITD is present in the envelope. Here we report the responses of neurons in the inferior colliculi of unanesthetized rabbits to ITDs of the envelopes of sinusoidally amplitude-modulated (SAM) tones. 2. Neurons were studied extracellularly with glass-coated Pt-Ir or Pt-W microelectrodes. Their sensitivity to ITDs in the envelopes of high-frequency sounds (greater-than-or-equal-to 2 kHz) was assessed using SAM tones that were presented binaurally. The tones at the two ears had the same carrier frequency but modulation frequencies that differed by 1 Hz. This caused a cyclic variation in the ITD produced by the envelope. In this ''binaural SAM'' stimulus, the carriers caused no ITD because they were in phase. In addition to the binaural SAM stimulus, pure tones were used to investigate responses to ipsilateral and contralateral stimulation and the nature of the interaction during binaural stimulation. 3. Neurons tended to display one of two kinds of sensitivity to ITDs. Some neurons discharged maximally at the same ITD at all modulation frequencies >250 Hz (peak-type neurons), whereas others were maximally suppressed at the same ITD (trough-type neurons). 4. At these higher modulation frequencies (>250 Hz), the characteristic delays that neurons exhibited tended to lie within the range that a rabbit might normally encounter (+/-300 mus). The peak-type neurons favored ipsilateral delays, which correspond to sounds in the contralateral sound field. The trough-type neurons showed no such preference. 5. The preference of peak-type neurons for a particular delay was sharper than that of trough-type neurons and was comparable to that observed in neurons of the inferior colliculus that are sensitive to delays of low-frequency pure tones. 6. At lower modulation frequencies (<150 Hz) characteristic delays often lay beyond +/-300 mus. 7. Increasing the ipsilateral intensity tended to shift the preferred delay ipsilaterally at lower (<250 Hz), but not at higher, modulation frequencies. 8. When tested with pure tones, a substantial number of peaktype neurons were found to be excited by contralateral stimulation but inhibited by ipsilateral stimulation. This is contrary to expectations, because the peak-type responses are believed to be inherited from the medial superior olive, where ipsilateral and contralateral excitatory inputs converge to generate a sensitivity to ITDs. 9. The last three observations indicate that many neurons process pure tones and slower modulations differently from more rapid modulations. These neurons may be specialized to process ITDs for sound localization only at higher modulation frequencies. In contrast, the responses to lower modulation frequencies may reflect the processing of interaural intensity differences.