Mechanisms Underlying Directional Selectivity for Frequency-Modulated Sweeps in the Inferior Colliculus Revealed by<i>In Vivo</i>Whole-Cell Recordings

Gittelman, Joshua X.; Li, Na; Pollak, George D.

doi:10.1523/jneurosci.2477-09.2009

Cited by 63 publications

(113 citation statements)

References 56 publications

(101 reference statements)

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“…Whole-cell patch recordings from visual cortical neurons showed, contrary to conclusions reached from pharmacologically blocking inhibition (34), that orientation selectivity can result from integration of excitatory thalamic inputs (35). Recent intracellular (particularly whole-cell) recordings have shown that biologically relevant stimuli can elicit diverse and complex patterns of excitation and inhibition in midbrain neurons (3,19,20,23,(36)(37)(38)(39)(40), suggesting that inhibition plays important computational roles. Our results provide direct evidence that GABA A antagonists can attenuate stimulusdriven inhibition and markedly reduce short-pass duration selectivity; bicuculline and the more selective GABA A antagonist, gabazine, had similar effects.…”

Section: Discussionmentioning

confidence: 97%

Phasic, suprathreshold excitation and sustained inhibition underlie neuronal selectivity for short-duration sounds

Alluri

Rose

Hanson

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Sound duration is important in acoustic communication, including speech recognition in humans. Although duration-selective auditory neurons have been found, the underlying mechanisms are unclear.To investigate these mechanisms we combined in vivo whole-cell patch recordings from midbrain neurons, extraction of excitatory and inhibitory conductances, and focal pharmacological manipulations. We show that selectivity for short-duration stimuli results from integration of short-latency, sustained inhibition with delayed, phasic excitation; active membrane properties appeared to amplify responses to effective stimuli. Blocking GABA A receptors attenuated stimulus-related inhibition, revealed suprathreshold excitation at all stimulus durations, and decreased short-pass selectivity without changing resting potentials. Blocking AMPA and NMDA receptors to attenuate excitation confirmed that inhibition tracks stimulus duration and revealed no evidence of postinhibitory rebound depolarization inherent to coincidence models of duration selectivity. These results strongly support an anticoincidence mechanism of short-pass selectivity, wherein inhibition and suprathreshold excitation show greatest temporal overlap for long duration stimuli.whole-cell | GABA | synaptic conductance | gabazine | inferior colliculus A principal goal in neuroscience is to understand the computational mechanisms that underlie selectivity for particular types of information. Sensory neurons have been identified that show selectivity for biologically relevant stimulus features; however, the underlying mechanisms are, in most cases, poorly understood. A notable exception involves mechanisms of selectivity for sound duration, particularly in bat and anuran auditory systems (1-3). Duration-selective neurons were first found in the midbrain torus semicircularis of anurans (4, 5), homolog of the mammalian inferior colliculus (IC) and referred to here as the IC an . In anurans and many mammalian species, midbrain neurons have been identified that show short-pass, band-pass, or long-pass duration selectivity (3, 6-11). These neurons code for temporal properties of acoustic signals that are important in communication and echolocation. Processing sound duration is also critical for human speech communication, and deficiencies in the neural processing of this and other temporal information feature prominently in disorders of speech recognition (12, 13). Hence, understanding the mechanisms of duration selectivity is of considerable importance.Several models of duration selectivity have been proposed. The first model, derived from extracellular recordings in the anuran IC (4), incorporates delayed, onset excitation and shortlatency offset excitation that coincide for the optimal stimulus duration (Fig. 1A). Subsequent extracellular recordings from IC neurons in bats showed that blocking receptors of inhibitory neurotransmitters eliminated, or greatly attenuated, duration selectivity (14-16). Further, the temporal pattern of discharges shifted from offset to onse...

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Section: Discussionmentioning

confidence: 97%

Phasic, suprathreshold excitation and sustained inhibition underlie neuronal selectivity for short-duration sounds

Alluri

Rose

Hanson

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Nothing is known of sweep selectivity at lower levels of the pallid bat auditory system, but in other species, direction and/or rate selectivity has been reported in the cochlear nucleus (Britt and Starr 1976;Godfrey et al 1975) and nuclei of the lateral lemniscus (Huffman et al 1998), as well as an extralemniscal region of the IC (Gordon and O'Neill 2000). The modeling of synaptic inputs to IC neurons further suggests that the inputs themselves may be selective for sweep direction and rate (Gittelman et al 2009). Grothe 1998).…”

Section: Discussionmentioning

confidence: 99%

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

Williams

Fuzessery

2011

Journal of Neurophysiology

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Williams AJ, Fuzessery ZM. Differential roles of GABAergic and glycinergic input on FM selectivity in the inferior colliculus of the pallid bat. J Neurophysiol 106: 2523-2535. First published July 20, 2011 doi:10.1152/jn.00569.2011.-Multiple mechanisms have been shown to shape frequency-modulated (FM) selectivity within the central nucleus of the inferior colliculus (IC) in the pallid bat. In this study we focus on the mechanisms associated with sideband inhibition. The relative arrival time of inhibition compared with excitation can be used to predict FM responses as measured with a two-tone inhibition paradigm. An early-arriving low-frequency inhibition (LFI) prevents responses to upward sweeps and thus shapes direction selectivity. A late-arriving high-frequency inhibition (HFI) suppresses slow FM sweeps and thus shapes rate selectivity for downward sweeps. Iontophoretic application of gabazine (GBZ) to block GABA A receptors or strychnine (Strych) to block glycine receptors was used to assess the effects of removal of inhibition on each form of FM selectivity. GBZ and Strych had a similar effect on FM direction selectivity, reducing selectivity in up to 86% of neurons when both drugs were coapplied. FM rate selectivity was more resistant to drug application with less than 38% of neurons affected. In addition, only Strych could eliminate FM rate selectivity, whereas GBZ alone was ineffective. The loss of FM selectivity was directly correlated to a loss of the respective inhibitory sideband that shapes that form of selectivity. The elimination of LFI correlated to a loss of FM direction selectivity, whereas elimination of HFI correlated to a loss of FM rate selectivity. Results indicate that 1) although the majority of FM direction selectivity is created within the IC, the majority of rate selectivity is inherited from lower levels of the auditory system, 2) a loss of LFI corresponds to a loss of FM direction selectivity and is created through either GABAergic or glycinergic input, and 3) a loss of HFI corresponds to a loss of FM rate selectivity and is created mainly through glycinergic input.

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“…Convergence of excitation and inhibition produces a host of response profiles in the central auditory system, including selectivity for stimulus frequency (Fuzessery and Hall, 1996;Wehr and Zador, 2003;Wu et al, 2008;Xie et al, 2008;Fukui et al, 2010), intensity , spatial position/sound localization (Rose et al, 1966;Fuzessery and Pollak, 1985;Zhang and Kelly, 2010;Tang et al, 2011), amplitude modulation (Grothe, 1994;Burger and Pollak, 1998), rhythm detection (Felix et al, 2011), FM sweep direction (Gittelman et al, 2009;Gittelman and Pollak, 2011), and pulse-echo delay (Galazyuk et al, 2005;Yavuzoglu et al, 2011). Inhibition shapes and sharpens neural responses by modulating the latency, strength, and time course of excitation.…”

Section: Duration Tuning and Other Auditory Feature Detectorsmentioning

confidence: 99%

“…Upward and downward FM sweeps evoke suprathreshold EPSPs of different magnitudes in IC neurons; however, IPSPs raise the spiking threshold of the cell to just below the largest excitatory input magnitude. This selects for only the strongest excitatory input and thus the corresponding FM sweep direction (Gittelman et al, 2009). Inhibitory inputs to DTNs are responsible for decreasing spike counts and sharpening temporal response profiles by increasing the spiking threshold of a neuron (Fig.…”

Section: Duration Tuning and Other Auditory Feature Detectorsmentioning

confidence: 99%

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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Mechanisms Underlying Directional Selectivity for Frequency-Modulated Sweeps in the Inferior Colliculus Revealed byIn VivoWhole-Cell Recordings

Cited by 63 publications

References 56 publications

Phasic, suprathreshold excitation and sustained inhibition underlie neuronal selectivity for short-duration sounds

Phasic, suprathreshold excitation and sustained inhibition underlie neuronal selectivity for short-duration sounds

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

Duration Tuning across Vertebrates

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