Intracellular Recording Reveals Temporal Integration in Inferior Colliculus Neurons of Awake Bats

Abstract

. The central nucleus of the inferior colliculus (IC) is a major integrative center in the central auditory system. It receives information from both the ascending and descending auditory pathways. To determine how single IC neurons integrate information over a wide range of sound frequencies and sound levels, we examined their intracellular responses to frequency-modulated (FM) sounds in awake little brown bats (Myotis lucifugus). Postsynaptic potentials were recorded in response to downward FM sweeps of the range typical for little brown bats (80 -20 kHz) and to three FM subcomponents . The majority of recorded neurons responded to the 80-to 20-kHz downward FM sweep with a complex response. In this response an initial hyperpolarization was followed by depolarization with or without spike followed by hyperpolarization. Intracellular recordings in response to three FM subcomponents revealed that these neurons receive excitatory and inhibitory inputs from a wide range of sound frequencies. One third of IC neurons performed nearly linear temporal summation across a wide range of sound frequencies, whereas two thirds of IC neurons exhibited nonlinear summation with different degrees of nonlinearity. Some IC neurons showed different latencies of postsynaptic potentials in response to different FM subcomponents. Often responses to the later FM subcomponent occurred before responses to the earlier ones. This phenomenon may be responsible for response selectivity of IC neurons to FM sweeps. I N T R O D U C T I O NNatural sounds, including animal communication sounds and human speech, contain both amplitude and frequency modulations (FM). This modulation creates a temporal structure that is a major source of information for sound recognition including speech (Shannon et al. 1995). Therefore it is important to understand how the auditory system extracts temporal information from complex sounds.Numerous studies using FM sounds have shown that the temporal structure of FM is reflected by neuronal responses in the auditory nerve and in lower auditory brain stem nuclei. At progressively higher levels of the auditory system, neurons become more selective for FM (review: Langner 1992). The inferior colliculus (IC), a large midbrain auditory processing center in vertebrates, contains neurons that are tuned to narrow ranges of modulation frequencies (Casseday et al. 1997;Langner and Schreiner 1988;Rees and Møller 1983;Schuller 1979).The first systematic study of FM response selectivity in IC neurons was performed in Myotis lucifugus (Suga 1968). Suga found a number of neurons that responded only to FM sweeps but not to pure tones. Similar results were reported later in the IC of other bats (Casseday and Covey 1992; Fuzessery 1994) and rats (Poon et al. 1992).A few possible neural mechanisms that can underlie FM rate and direction tuning in IC neurons of mustached and pallid bats were previously proposed (Brimijoin and O'Neill 2005;Fuzessery et al. 2006;Heil et al. 1992;Rall 1964;Suga 1965;Suga and Schlegel 1973). The sideband in...

Rethinking Tuning:In VivoWhole-Cell Recordings of the Inferior Colliculus in Awake Bats

“…To be sure, the responses on the far frequency flanks of the tuned regions in most cells were mainly IPSPs, but, as pointed out previously, we cannot be sure that those events were purely inhibitory or were composed of a much stronger inhibition that swamped a weaker excitation. Either way, the synaptic tuning in the majority of IC cells is not reflected in the expanded discharge tuning during blocking inhibition but rather shows that many IC cells receive innervation from inputs that have a broader spectral range than previously believed, a feature also seen in a recent intracellular study of responses to FM sweeps (Voytenko and Galazyuk, 2007). …”

“…Two studies used either clicks (Pedemonte et al, 1997) or FM sweeps (Voytenko and Galazyuk, 2007), and two others only report that tones evoked PSPs in all cells but do not comment on whether or not all of those cells also discharged to tones (Nelson and Erulkar, 1963;Kuwada et al, 1997). In the whole-cell study by Covey et al (1996), the patch electrodes were filled with cesium, which influenced excitability.…”

“…Inhibition can only be directly visualized with intracellular recordings. Over the past four decades, however, there have been only a few in vivo intracellular studies of the IC that used either sharp electrodes (Nelson and Erulkar, 1963;Kuwada et al, 1997;Pedemonte et al, 1997;Voytenko and Galazyuk, 2007) or whole-cell recordings Covey et al, 1996;. Al-though those studies have shown the prevalence of sound-evoked inhibition in the IC with both monaural and binaural stimulation, the stimuli used to evoke responses in all of those studies used clicks, amplitude modulations, FM sweeps, or best frequency (BF) tones, the frequency to which the neuron is most sensitive, and only rarely were responses to additional off-BF frequencies presented.…”

Differential roles of GABAergic and glycinergic input on FM selectivity in the inferior colliculus of the pallid bat

“…10). In general, the frequency tuning of inhibitory inputs are thought to roughly match their excitatory tuning (Palombi and Caspary 1996), since the frequencies of the inhibitory sidebands vary with a neuron's best excitatory frequency, although the spectral bandwidth of inhibitory inputs can be considerably wider than the excitatory inputs (Voytenko and Galazyuk 2007;Xie et al 2007).…”

Phoneme and word recognition in the auditory ventral stream

“…In the case of speech sounds, these neurons conjoin representations for adjacent speech formants or, at higher levels, adjacent phonemes. Although the mechanism by which combination sensitivity (CS) is directionally selective in the temporal domain is not fully understood, some propositions exist (22)(23)(24)(25)(26). As an empirical matter, direction selectivity is clearly present early in auditory cortex (19,27).…”