Contribution of NMDA and AMPA Receptors to Temporal Patterning of Auditory Responses in the Inferior Colliculus

Sanchez, Jason Tait; Gans, Donald; Wenstrup, Jeffrey J.

doi:10.1523/jneurosci.2894-06.2007

Cited by 40 publications

(41 citation statements)

References 46 publications

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“…For shorter latency neurons, AMPA receptors play a more dominant role. NMDA receptors may also contribute to the latencies of long-latency neurons in the IC through their slower activation kinetics (Sanchez et al, 2007). The current study provides evidence that long-latency neurons are also especially sensitive to serotonergic modulation.…”

Section: Characteristics and Roles Of Long-latency Neuronsmentioning

confidence: 57%

Activation of the serotonin 1A receptor alters the temporal characteristics of auditory responses in the inferior colliculus

Hurley

2007

Brain Research

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Serotonin, like other neuromodulators, acts on a range of receptor types, but its effects also depend on the functional characteristics of the neurons responding to receptor activation. In the inferior colliculus (IC), an auditory midbrain nucleus, activation of a common serotonin (5-HT) receptor type, the 5-HT 1A receptor, depresses auditory-evoked responses in many neurons. Whether these effects occur differentially in different types of neurons is unknown. In the current study, the effects of iontophoretic application of the 5-HT 1A agonist 8-OH-DPAT on auditory responses were compared with the characteristic frequencies (CFs), recording depths, and control first-spike latencies of the same group of IC neurons. The 8-OH-DPAT-evoked change in response significantly correlated with first-spike latency across the population, so that response depressions were more prevalent in longer-latency neurons. The 8-OH-DPAT-evoked change in response did not correlate with CF or with recording depth. 8-OH-DPAT also altered the temporal characteristics of spike trains in a subset of neurons that fired multiple spikes in response to brief stimuli. For these neurons, activation of the 5-HT 1A receptor suppressed lagging spikes proportionally more than initial spikes. These results suggest that the 5-HT 1A receptor, by affecting the timing of the responses of both individual neurons and the neuron population, shifts the temporal profile of evoked activity within the IC.

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Section: Characteristics and Roles Of Long-latency Neuronsmentioning

confidence: 57%

Activation of the serotonin 1A receptor alters the temporal characteristics of auditory responses in the inferior colliculus

Hurley

2007

Brain Research

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“…All procedures were approved by the Institutional Animal Care and Use Committees at the Northeastern Ohio Universities College of Medicine and Kent State University. Most procedures used here are identical to our previous study of the role of glutamate receptors in responses of IC neurons to single tones (Sanchez et al, 2007).…”

Section: Methodsmentioning

confidence: 99%

“…Recordings and microiontophoresis were similar to previous experiments (Nataraj and Wenstrup, 2005;Sanchez et al, 2007). Briefly, physiologic experiments were conducted in a single-walled Industrial Acoustics (New York, NY) chamber lined with polyurethane foam to reduce echoes.…”

Section: Methodsmentioning

confidence: 99%

“…Other barrels were filled with the AMPA/kainate receptor antagonist 1,2,3,4-tetrahydro-6-nitro-2,3-dioxo-benzo[f]quinoxaline-7-sulfonamide (NBQX) (5 mM, pH 9.0, vehicle 0.9% physiologic saline; Sigma, St. Louis, MO), the NMDA receptor antagonist (Ϯ)-3-(2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid (CPP) (10 mM, pH 8.0, vehicle 0.9% physiologic saline), the GABA A receptor (GABA A R) antagonists bicuculline (10 mM, pH 3.0, vehicle 0.9% physiologic saline; Sigma) or gabazine (SR95531, 3 mM, pH 4.0, vehicle 0.9% physiologic saline; Tocris Bioscience, Ellisville, MO), and the glycine receptor (GlyR) antagonist strychnine (10 mM, pH 3.0, vehicle 0.9% physiologic saline; Fluka, Milwaukee, WI). The rationale for our choice of glutamate blockers was described previously (Sanchez et al, 2007).…”

Section: Methodsmentioning

confidence: 99%

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Glycinergic “Inhibition” Mediates Selective Excitatory Responses to Combinations of Sounds

2008

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In the mustached bat's inferior colliculus (IC), combination-sensitive neurons display time-sensitive facilitatory interactions between inputs tuned to distinct spectral elements in sonar or social vocalizations. Here we compare roles of ionotropic receptors to glutamate (iGluRs), glycine (GlyRs), and GABA (GABA A Rs) in facilitatory combination-sensitive interactions. Facilitatory responses to 36 single IC neurons were recorded before, during, and after local application of antagonists to these receptors. The NMDA receptor antagonist CPP [(Ϯ)-3-(2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid], alone (n ϭ 14) or combined with AMPA receptor antagonist NBQX (n ϭ 22), significantly reduced or eliminated responses to best frequency (BF) sounds across a broad range of sound levels, but did not eliminate combination-sensitive facilitation. In a subset of neurons, GABA A R blockers bicuculline or gabazine were applied in addition to iGluR blockers. GABA A R blockers did not "uncover" residual iGluR-mediated excitation, and only rarely eliminated facilitation. In nearly all neurons for which the GlyR antagonist strychnine was applied in addition to iGluR blockade (22 of 23 neurons, with or without GABA A R blockade), facilitatory interactions were eliminated. Thus, neither glutamate nor GABA neurotransmission are required for facilitatory combination-sensitive interactions in IC. Instead, facilitation may depend entirely on glycinergic inputs that are presumed to be inhibitory. We propose that glycinergic inputs tuned to two distinct spectral elements in vocal signals each activate postinhibitory rebound excitation. When rebound excitations from two spectral elements coincide, the neuron discharges. Excitation from glutamatergic inputs, tuned to the BF of the neuron, is superimposed onto this facilitatory interaction, presumably mediating responses to a broader range of acoustic signals.

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“…For example, when we set the g NMDA to 6 nS, the model DTN switched from offset responding to onset responding when the g NMDA was only 55 nS (data not shown). This highlights how the spiking response pattern of a neuron can be mediated by a complex interaction of solely excitatory currents (Zhang and Kelly, 2001;Sanchez et al, 2007).…”

Section: Maximum Receptor Conductancementioning

confidence: 97%

Duration Tuning across Vertebrates

Aubie

Sayegh²,

Faure³

2012

J. Neurosci.

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Signal duration is important for identifying sound sources and determining signal meaning. Duration-tuned neurons (DTNs) respond preferentially to a range of stimulus durations and maximally to a best duration (BD). Duration-tuned neurons are found in the auditory midbrain of many vertebrates, although studied most extensively in bats. Studies of DTNs across vertebrates have identified cells with BDs and temporal response bandwidths that mirror the range of species-specific vocalizations. Neural tuning to stimulus duration appears to be universal among hearing vertebrates. Herein, we test the hypothesis that neural mechanisms underlying duration selectivity may be similar across vertebrates. We instantiated theoretical mechanisms of duration tuning in computational models to systematically explore the roles of excitatory and inhibitory receptor strengths, input latencies, and membrane time constant on duration tuning response profiles. We demonstrate that models of duration tuning with similar neural circuitry can be tuned with species-specific parameters to reproduce the responses of in vivo DTNs from the auditory midbrain. To relate and validate model output to in vivo responses, we collected electrophysiological data from the inferior colliculus of the awake big brown bat, Eptesicus fuscus, and present similar in vivo data from the published literature on DTNs in rats, mice, and frogs. Our results support the hypothesis that neural mechanisms of duration tuning may be shared across vertebrates despite species-specific differences in duration selectivity. Finally, we discuss how the underlying mechanisms of duration selectivity relate to other auditory feature detectors arising from the interaction of neural excitation and inhibition.

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Contribution of NMDA and AMPA Receptors to Temporal Patterning of Auditory Responses in the Inferior Colliculus

Cited by 40 publications

References 46 publications

Activation of the serotonin 1A receptor alters the temporal characteristics of auditory responses in the inferior colliculus

Activation of the serotonin 1A receptor alters the temporal characteristics of auditory responses in the inferior colliculus

Glycinergic “Inhibition” Mediates Selective Excitatory Responses to Combinations of Sounds

Duration Tuning across Vertebrates

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