Glycinergic Inhibition Creates a Form of Auditory Spectral Integration in Nuclei of the Lateral Lemniscus

Abstract

For analyses of complex sounds, many neurons integrate information across different spectral elements via suppressive effects that are distant from the neurons' excitatory tuning. In the mustached bat, suppression evoked by sounds within the first sonar harmonic (23-30 kHz) or in the subsonar band (<23 kHz) alters responsiveness to the higher best frequencies of many neurons. This study examined features and mechanisms associated with low-frequency (LF) suppression among neurons of the lateral lemniscal nuclei (NLL). We obtained extracellular recordings from neurons in the intermediate and ventral nuclei of the lateral lemniscus, observing different forms of LF suppression related to the two above-cited frequency bands. To understand the mechanisms underlying this suppression in NLL neurons, we examined the roles of glycinergic and GABAergic input through local microiontophoretic application of strychnine, an antagonist to glycine receptors (GlyRs), or bicuculline, an antagonist to gamma-aminobutyric acid type A receptors (GABA(A)Rs). With blockade of GABA(A)Rs, neurons showed an increase in firing rate to best frequency (BF) and/or LF tones but retained LF suppression of BF sounds. For neurons that displayed LF suppression tuned to 23-30 kHz, the suppression was eliminated or nearly eliminated by GlyR blockade. In contrast, GABA(A)R blockade did not eliminate nor had any consistent effect on suppression tuned to these frequencies. We conclude that LF suppression tuned in the 23- to 30-kHz range results from neuronal inhibition within the NLL via glycinergic inputs. For neurons displaying suppression tuned <23 kHz, neither GlyR nor GABAR blockade altered LF suppression. We conclude that such suppression originates at a lower auditory level, perhaps a result of cochlear mechanisms. These findings demonstrate that neuronal interactions within NLL create a particular form of LF suppression that contributes to the analysis of complex acoustic signals.

Substrates of auditory frequency integration in a nucleus of the lateral lemniscus

“…At all combination-sensitive tracer deposit sites, inhibition was best at simultaneous presentation. These responses are consistent with features of combination-sensitive inhibition in INLL that are mediated by low frequency glycinergic input (Peterson et al, 2009). …”

“…Neurons were considered to show low frequency inhibition of high-BF signals if the low frequency tone suppressed the excitatory response to the BF tone by at least 20%. These criteria are consistent with features of combination sensitivity in INLL that depend on glycinergic inhibition (Peterson et al, 2009). In experiments featuring tracer deposits tuned to BFs in the 23–30 kHz range, only frequency response and rate-level functions were obtained.…”

“…Electrophysiological recordings were similar to those described in a previous study of the lateral lemniscal nuclei (Peterson et al, 2009). The bat was placed within a custom-made stereotaxic apparatus housed in a single-walled Industrial Acoustic chamber (New York, NY), lined with polyurethane foam to reduce echoes.…”

“…Inhibitory combination-sensitive responses in INLL require excitatory inputs tuned to the neuron’s high BF and a glycinergic input tuned at least an octave lower in frequency (Peterson et al, 2009). The results describe circuitry that could underlie this complex response.…”

“…Many neurons in the auditory midbrain, thalamus, and forebrain of this bat display a form of temporally sensitive spectral integration called combination sensitivity, in which the neuron’s excitatory response to one frequency band is inhibited or facilitated by another frequency element that is one to three octaves lower (Suga et al, 1978; O’Neill and Suga, 1979; O’Neill, 1985; Olsen and Suga, 1991; Mittmann and Wenstrup, 1995; Wenstrup, 1999). While the facilitatory interaction originates within the midbrain’s inferior colliculus (IC) (Portfors and Wenstrup, 2001; Wenstrup and Leroy, 2001, Nataraj and Wenstrup, 2005; Marsh et al, 2006), the inhibitory spectral interaction originates within the intermediate and ventral nuclei of the lateral lemniscus and depends on low frequency-tuned glycinergic inhibition of high-frequency-tuned excitatory responses (Peterson et al, 2009). The present study examines the source of this low-frequency, glycinergic input to provide evidence of a spectrally integrative circuit within the auditory brainstem.…”