Sound localization: Jeffress and beyond

Abstract

Many animals use the interaural time differences (ITDs) to locate the source of low frequency sounds. The place coding theory proposed by Jeffress has long been a dominant model to account for the neural mechanisms of ITD detection. Recent research, however, suggests a wider range of strategies for ITD coding in the binaural auditory brainstem. We discuss how ITD is coded in avian, mammalian, and reptilian nervous systems, and review underlying synaptic and cellular properties that enable precise temporal computation. The latest advances in recording and analysis techniques provide powerful tools for both overcoming and utilizing the large field potentials in these nuclei.

Figure 1. Various ITD coding strategies

A. Chicken’s ITD coding circuit. (Left) Schematic drawing of the chicken’s brainstem. Axons from the ipsilateral NM enter NL dorsally, while those from contralateral NM enter ventrally. NL neurons are aligned in a thin flat layer. (Center) Jeffress-type organization of the chicken’s NM-NL circuit. Axonal conduction times lead to a place map in NL. Neurons near the lateral border of NL (marked as C ) response maximally to sounds coming from the far contralateral side, and cells located close to the medial edges of NL (marked as F ) fires maximally to sounds originating from in front of the animal’s head. (Right) Example ITD-response curves of NL cells tuned at 1 kHz. As stated above, the peak position of the tuning curve depends on the location of the neuron in the place map. Positive ITD values mean contralateral ear leading (i.e., sound arrives earlier at the contralateral ear than at the ipsilateral ear). B. Owl’s ITD coding circuit. (Left) Schematic drawing of the owl’s brainstem. Similar to the chicken brainstem, axons from the ipsilateral NM enter NL dorsally, while those from contralateral NM enter ventrally. Owl NL neurons, however, are not aligned in a layered structure, but are distributed sparsely throughout the nucleus. (Center) Multiple Jeffress-type place maps of the owl’s NM-NL circuit. Gradual changes in axonal conduction times along the dorsoventral dimension result in multiple place maps of NL cells. Neurons near the dorsal border of NL (marked as “C”) response maximally to sounds coming from the far contralateral side, and cells located close to the ventral edges of NL (marked as “F”) fires maximally to sounds originating from in front of the animal’s head. (Right) Example ITD-response curves of NL cells tuned at 5 kHz. As in chickens place map, the peak position of the tuning curve depends on the location of the neuron in the place map. C. Gerbil’s ITD coding circuit. (Left) Schematic drawing of the gerbil’s brainstem. Spherical bushy cells in the VCN provide excitatory inputs to the MSO, while LNTB and MNTB neurons, which receive outputs of the globular bushy cells in the ipsi- and contralateral VCN, respectively, send glycinergic inhibitory inputs to MSO. (Center) Schematic picture of a gerbil MSO neuron. The principal neuron of the MSO has bipolar dendrites segregating ipsi- and contralateral excitatory inputs from the VCN. Inhibitory inputs from LNTB and MNTB are confined to the cell body region. (Right) Example ITD-response curves of MSO cells tuned at 1 kHz. In contrast to chicken’s NL cells, the tuning curves of MSO neurons are very similar. Peak positions of the tuning curves can lie out of the physiological ITD range (i.e., ITDs encountered naturally) shown by the shaded area. D. Gecko’s ITD coding. (Left) Schematic drawing of the gecko’s head. The inner ears of the gecko are interconnected through the mouth cavity. (Center) Gecko’s ear as a pressure gradient receiver. Sound wave arriving at one ear travels through the mouth cavity to reach the tympanic membrane (eardrum) of the other ear, resulting in binaural sound interactions. The motion amplitude of the eardrum changes with the phase difference between the two sounds from inside and outside the ear. (Right) Example ITD-response curves of auditory nerves tuned at 2 kHz. ITD-dependent changes in the motion amplitude of the tympanic membrane results in the spike rate modulation of the auditory nerve in an ITD-dependent manner. Note that the trough of the ITD-response curve at around 200–250 ms corresponds to the conduction delay of sound through the mouth cavity. Abbreviations: AN, auditory nerve; NA, nucleus angularis; NM, nucleus magnocellularis; NL, nucleus laminaris; VCN, ventral cochlear nucleus; LNTB, lateral nucleus of the trapezoid body; MNTB, medial nucleus of the trapezoid body; MSO, medial superior olive. A (left and center), B (left and center) modified from [77]; C (left and center) modified from [9]; D (left) modified from [13*].