Monaural interaction of excitation and inhibition in the medial superior olive of the mustached bat: an adaptation for biosonar.

Abstract

In most mammals, the superior olive is the first stage for binaural interaction. Neurons in the medial superior olive (MSO) receive excitatory input from both ears and are sensitive to interaural time or phase differences of low-frequency sounds. The mustached bat (Pteronotusparnelli parneffii), a small echolocating species with high-frequency hearing, probably does not use interaural time or phase differences as cues for sound localization. Although the mustached bat has a large MSO, there is some evidence that it is functionally different from the MSO in nonecholocating mammals. Most MSO neurons in the mustached bat are monaural, excited by a contralateral sound. Their responses are phasic and correlated with either the onset or the offset of a sound. As a first step in determining the origin of these phasic monaural responses, we traced the connections of the MSO by using both retrograde and anterograde transport methods. Excitatory inputs to the MSO originate from spherical cells in the anteroventral cochlear nucleus, almost exclusively from the contralateral side. Glycinergic inhibitory input is relayed from the contralateral cochlear nucleus through the medial nucleus of the trapezoid body. To investigate the interactions of the contralateral excitatory and inhibitory inputs at the level of the MSO cell, we recorded sound-evoked responses and applied glycine or its antagonist by using microiontophoresis. The results show that the phasic response to a contralateral sound is created by interaction of a sustained excitatory input with a sustained inhibitory input, also from the contralateral ear. Whether the response is to the onset or offset of a sound is determined by the relative timing between the excitatory and inhibitory inputs. Thus, in MSO of the mustached bat, the ipsilateral excitatory pathway from the cochlear nucleus seen in animals with low-frequency hearing is virtually absent, and the MSO is adapted for timing analysis by using input from only the contralateral ear.The mammalian superior olivary complex is the first stage at which there is convergence of inputs from the two ears. The current view of its function is that it provides two parallel pathways to the auditory midbrain, each of which is specialized to compare sound at the two ears and transmit basic information necessary for sound localization. In this scheme, neurons in the lateral superior olive (LSO) are selective for interaural sound level differences and neurons in the medial superior olive (MSO) are selective for interaural time or phase differences (1, 2).This view of MSO function is based mainly on data obtained in mammals with large heads and good lowfrequency hearing. Species with small heads and highfrequency hearing probably do not have interaural time or phase differences in a range that would be useful for sound localization, and in some cases they appear to lack an MSO (1, 3, 4). However, in other cases, notably in echolocating bats, a large MSO is present despite a small head size and high-frequency hearing rang...

Anatomy and projection patterns of the superior olivary comlex in the mexican free‐tailed bat, Tadarida brasiliensis mexicana

“…An extreme modification of this sort is seen in the MSO of the mustached bat. The characteristics of the MSO in this bat are similar to those of other mammals, but the ipsilateral inputs are reduced or absent, and the inhibitory inputs from the MNTB are enlarged (Grothe, 1990;Covey et al, 1991;Grothe et al, 1992;Vater, 1993). The MSO neurons are, thus, monaural, but their responses depend on the timing of the excitatory and inhibitory inputs they receive from the contralateral ear, The nature of this dependency is highly similar to that seen in the brain slices of the gerbil MSO neurons when driven with contralateral stimulation (Grothe and Sanes, 1994).…”

“…However, it leaves unanswered the question of why molossid bats employ these two nuclei for binaural processing of localization information, while other bats have only a vestigial (Irving and Harrison, 1967) or a monaural MSO (Grothe et al, 1992).…”

“…Through modifying the degree of excitatory and inhibitory innervation, the coding features of MSO neurons could be adjusted (Grothe et al, 1992;Grothe and Sanes, 1994). An extreme modification of this sort is seen in the MSO of the mustached bat.…”

“…However, these neurons utilize timing differences between the excitatory inputs from the cochlear nucleus and inhibitory inputs from the MNTB, in a manner similar to those proposed for the processing of interaural phase disparities. The difference is the absence of an input from the ipsilateral ear, thereby producing monaural response features of biological importance to the animal (Grothe, 1990(Grothe, , 1994Covey et al, 1991;Grothe et al, 1992).…”

The functional role of GABA and glycine in monaural and binaural processing in the inferior colliculus of horseshoe bats

“…This effect can be explained by the relative timing of excitatory and inhibitory inputs (see also Grothe et al 1992) and/or by differences in rise time and strength of simultaneously arriving excitatory and inhibitory postsynaptic potentials. A change from phasic-on to tonic response activity under the influence of bicuculline suggests that the neuron receives a tonic excitatory input, whose late component is suppressed by an additional GABAergic input.…”