Reversible Inactivation of the Dorsal Nucleus of the Lateral Lemniscus Reveals Its Role in the Processing of Multiple Sound Sources in the Inferior Colliculus of Bats

Abstract

Neurons in the inferior colliculus (IC) that are excited by one ear and inhibited by the other [excitatory-inhibitory (EI) neurons] can code interaural intensity disparities (IIDs), the cues animals use to localize high frequencies. Although EI properties are first formed in a lower nucleus and imposed on some IC cells via an excitatory projection, many other EI neurons are formed de novo in the IC. By reversibly inactivating the dorsal nucleus of the lateral lemniscus (DNLL) in Mexican free-tailed bats with kynurenic acid, we show that the EI properties of many IC cells are formed de novo via an inhibitory projection from the DNLL on the opposite side. We also show that signals excitatory to the IC evoke an inhibition in the opposite DNLL that persists for tens of milliseconds after the signal has ended. During that period, strongly suppressed EI cells in the IC are deprived of inhibition from the DNLL and respond to binaural signals as weakly inhibited or monaural cells. By relieving inhibition at the IC, we show that an initial binaural signal essentially reconfigures the circuit and thereby allows IC cells to respond to trailing binaural signals that were inhibitory when presented alone. Thus, DNLL innervation creates a property in the IC that is not possessed by lower neurons or by collicular EI neurons that are not innervated by the DNLL. That property is a change in responsiveness to binaural signals, a change dependent on the reception of an earlier sound. These features suggest that the circuitry linking the DNLL with the opposite central nucleus of the IC is important for the processing of IIDs that change over time, such as the IIDs generated by moving stimuli or by multiple sound sources that emanate from different regions of space. Key words: GABA; persistent inhibition; precedence effect; inferior colliculus; sound localization; dorsal nucleus of lateral lemniscusThe projections from the vast majority of lower auditory nuclei converge at a common destination in the central nucleus of the inferior colliculus (ICc) (for review, see Aitkin, 1986;Oliver and Huerta, 1992). This large convergence of inputs suggests that substantial transformations occur in the ICc; yet the response properties of ICc neurons appear to be similar to those of the lower nuclei from which they receive their innervation. An example is excitatory-inhibitory (EI) neurons in the ICc, neurons that are excited by one ear and inhibited by the other ear. These neurons are sensitive to interaural intensity disparities (IIDs), the cues animals use to localize high-frequency sounds (Erulkar, 1972;Mills, 1972). EI neurons are initially formed in the lateral superior olive (LSO) (Boudreau and Tsuchitani, 1968;Finlayson and Caspary, 1991). They are also the dominant type in the dorsal nucleus of the lateral lemniscus (DNLL), a nucleus the neurons of which are almost exclusively GABAergic (Brugge et al., 1970;Adams and Mugniani, 1984;Covey, 1993; Yang and Pollak, 1994a,b,c;Winer et al., 1995). The DNLL, like the ICc, is one of the principa...

Inhibiting the Inhibition: A Neuronal Network for Sound Localization in Reverberant Environments

“…These features are consistent with a previous study that determined responses to initial and trailing sounds in EI cells that are innervated by the DNLL in the IC of bats (Burger and Pollak, 2001). We used the model to investigate how the IC response patterns changed when PI was not incorporated as an intrinsic feature of the DNLL-DNLL interaction.…”

“…This causes the suppression of lagging sounds that would normally evoke discharges. We suggest that PI is a feature of the auditory system in all mammals, because it now has been described in rodents (this study) as well as in bats (Yang and Pollak, 1994a;Burger and Pollak, 2001). Our in vitro recordings infer that PI is a feature of the GABAergic transmission of the commissure of Probst and, for the first time, imply a cellular basis for PI.…”

“…1, 4 A). The model was restricted to a specific population of IC neurons, as described by pharmacological studies (Li and Kelly, 1992;Burger and Pollak, 2001): these IC cells receive an excitatory projection from the contralateral AVCN in combination with an inhibitory projection from the contralateral DNLL. This interaction creates EI properties, and hence IID sensitivity, in the IC de novo.…”

“…First, many DNLL neurons respond to sounds from the contralateral ear but are inhibited by sounds from the ipsilateral ear and thus are sensitive to interaural intensity differences (IIDs), a feature they inherit from the lateral superior olive (LSO) (Glendenning et al, 1981;Shneiderman et al, 1988). Second, in bats, DNLL neurons display an additional characteristic not known from the LSO: depending on the spatiotemporal succession of stimuli, their response can be suppressed for tens of milliseconds as a result of GABAergic inhibition Pollak, 1994a,b, 1998;Burger and Pollak, 2001). It has been hypothesized that such "persistent inhibition" (PI) is derived from the opposite DNLL via the commissure of Probst (Yang and Pollak, 1998) (Fig.…”

Dynamic changes in level influence spatial coding in the lateral superior olive

“…In one study, precedence-like effect in collicular neurons was blocked by reversibly inactivating the dorsal nucleus of the lateral lemniscus, a strong source of GABAergic inhibition to the inferior colliculus (Burger and Pollak, 2001). Similarly, Sanes et al (1998) showed that collicular neurons displayed a paradoxical after-effect both from changing ILD and from a brief local application of inhibitory transmitter.…”