IID sensitivity differs between two principal centers in the interaural intensity difference pathway: the LSO and the IC

J Neurophysiol. 1998 May;79(5):2416-31. doi: 10.1152/jn.1998.79.5.2416.

Abstract

Interaural intensity differences (IIDs) are the chief cues that animals use to localize high-frequency sounds. Neurons that are sensitive to IIDs are excited by sound at one ear and inhibited by sound at the other. Thus a given IID generates a combination of excitation and inhibition that is reflected in a cell's spike count. In mammals, the so-called "IID pathway" begins in the lateral superior olive (LSO), which is dominated by the type of IID-sensitive neurons just described. The LSO then sends a prominent projection to the inferior colliculus (IC), which also contains a substantial population of IID-sensitive cells. Recent pharmacological studies have suggested that the response properties of IID-sensitive neurons in the IC undergo considerable processing and thus should not simply reflect the output of the LSO. However, we have no direct evidence as to whether IID sensitivity, the defining response feature of these cells, differs at these two levels. The present study makes this direct comparison in the Mexican free-tailed bat, a species that relies greatly on high-frequency hearing and thus on IIDs for localizing sounds in space. Extracellular recording techniques were used to obtain IID functions from 50 IC neurons. Comparable data from 50 LSO cells were available from a previous study. The main result was that IID sensitivity significantly differed between cells in the LSO and the IC. Among LSO cells, sensitivity was centered approximately 0 dB (no intensity difference between the ears) whereas, in the IC, sensitivity was biased toward the inhibitory ear: on average, IC cells required a more intense signal at the inhibitory ear to reach the same degree of suppression as observed in LSO cells. Further analysis showed that the vast majority of IC cells (88%) exhibited a mismatch in the latencies of their inputs: inhibition arrived later when an equally strong excitation and inhibition were elicited; this reduced the effectiveness of the inhibition. Because latency shortens with increasing stimulus intensity, an IID with a more intense signal at the inhibitory ear could equate the latencies of excitation and inhibition, increasing the effectiveness of the inhibition. This result suggests that latency mismatches account, to a great extent, for the difference in sensitivity between the LSO and the IC; and when mismatches were negated by electronically time shifting the signals to the ears, sensitivity was no longer significantly different between the two nuclei.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Acoustic Stimulation
  • Action Potentials
  • Animals
  • Auditory Pathways / physiology*
  • Auditory Threshold
  • Chiroptera / physiology*
  • Echolocation / physiology*
  • Inferior Colliculi / cytology
  • Inferior Colliculi / physiology*
  • Neurons / physiology
  • Olivary Nucleus / cytology
  • Olivary Nucleus / physiology*
  • Reaction Time