. 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...
Peterson DC, Voytenko S, Gans D, Galazyuk A, Wenstrup J. Intracellular recordings from combination-sensitive neurons in the inferior colliculus. J Neurophysiol 100: 629-645, 2008. First published May 21, 2008 doi:10.1152/jn.90390.2008. In vertebrate auditory systems, specialized combination-sensitive neurons analyze complex vocal signals by integrating information across multiple frequency bands. We studied combinationsensitive interactions in neurons of the inferior colliculus (IC) of awake mustached bats, using intracellular somatic recording with sharp electrodes. Facilitated combinatorial neurons are coincidence detectors, showing maximum facilitation when excitation from low-and high-frequency stimuli coincide. Previous work showed that facilitatory interactions originate in the IC, require both low and high frequency-tuned glycinergic inputs, and are independent of glutamatergic inputs. These results suggest that glycinergic inputs evoke facilitation through either postinhibitory rebound or direct depolarizing mechanisms. However, in 35 of 36 facilitated neurons, we observed no evidence of low frequency-evoked transient hyperpolarization or depolarization that was closely related to response facilitation. Furthermore, we observed no evidence of shunting inhibition that might conceal inhibitory inputs. Since these facilitatory interactions originate in IC neurons, the results suggest that inputs underlying facilitation are electrically segregated from the soma. We also recorded inhibitory combinatorial interactions, in which low frequency sounds suppress responses to higher frequency signals. In 43% of 118 neurons, we observed low frequency-evoked hyperpolarizations associated with combinatorial inhibition. For these neurons, we conclude that low frequency-tuned inhibitory inputs terminate on neurons primarily excited by high-frequency signals; these inhibitory inputs may create or enhance inhibitory combinatorial interactions. In the remainder of inhibited combinatorial neurons (57%), we observed no evidence of low frequency-evoked hyperpolarizations, consistent with observations that inhibitory combinatorial responses may originate in lateral lemniscal nuclei.
Neurons in the inferior colliculus (IC), one of the major integrative centers of the auditory system, process acoustic information converging from almost all nuclei of the auditory brain stem. During this integration, excitatory and inhibitory inputs arrive to auditory neurons at different time delays. Result of this integration determines timing of IC neuron firing. In the mammalian IC, the range of the first spike latencies is very large (5-50 ms). At present, a contribution of excitatory and inhibitory inputs in controlling neurons' firing in the IC is still under debate. In the present study we assess the role of excitation and inhibition in determining first spike response latency in the IC. Postsynaptic responses were recorded to pure tones presented at neuron's characteristic frequency or to downward frequency modulated sweeps in awake bats. There are three main results emerging from the present study: (1) the most common response pattern in the IC is hyperpolarization followed by depolarization followed by hyperpolarization, (2) latencies of depolarizing or hyperpolarizing responses to tonal stimuli are short (3-7 ms) whereas the first spike latencies may vary to a great extent (4-26 ms) from one neuron to another, and (3) high threshold hyperpolarization preceded long latency spikes in IC neurons exhibiting paradoxical latency shift. Our data also show that the onset hyperpolarizing potentials in the IC have very small jitter (<100 micros) across repeated stimulus presentations. The results of this study suggest that inhibition, arriving earlier than excitation, may play a role as a mechanism for delaying the first spike latency in IC neurons.
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