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

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

doi:10.1523/jneurosci.3572-07.2008

Cited by 51 publications

(75 citation statements)

References 41 publications

(68 reference statements)

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“…Facilitatory interactions in IC are always eliminated or nearly eliminated through blockade of glycine receptors in IC (Nataraj and Wenstrup 2005;Sanchez et al 2008;Wenstrup and Leroy 2001). These results strongly suggest that every facilitated combination-sensitive response in the IC is the result of interactions of glycinergic inputs onto the facilitated IC neurons.…”

Section: Combination-sensitive Facilitatory Interactions May Occur Wimentioning

confidence: 79%

“…Such results suggest that the use of FM sweeps rather than tonal signals did not fundamentally alter combination-sensitive interactions. Wenstrup 2005;Sanchez et al 2008;Wenstrup and Leroy 2001), we examined intracellular responses to both low-frequency and high-frequency facilitating signals for soundevoked hyperpolarizing potentials. Our major observations were that most facilitated neurons showed no evidence of low frequency-evoked hyperpolarizations but occasionally showed evidence of high frequency-evoked hyperpolarizations.…”

Section: R E S U L T Smentioning

confidence: 99%

“…Such facilitation does not occur in auditory brain stem structures (Marsh et al 2006;Portfors and Wenstrup 2001) but instead seems to originate in high-frequency regions of the IC (Nataraj and Wenstrup 2005;Wenstrup and Leroy 2001;Wenstrup et al 1999). Recent work has shown that response facilitation in IC neurons is independent of glutamatergic inputs but requires glycinergic inputs (Sanchez et al 2008). Glycine-dependant facilitation may result from a postinhibitory rebound mechanism (Nataraj and Wenstrup 2005), in which both low-and high-frequency glycinergic inputs generate inhibitory postsynaptic potentials (IPSPs) followed by rebound excitation (Sanchez et al 2008).…”

mentioning

confidence: 99%

“…Recent work has shown that response facilitation in IC neurons is independent of glutamatergic inputs but requires glycinergic inputs (Sanchez et al 2008). Glycine-dependant facilitation may result from a postinhibitory rebound mechanism (Nataraj and Wenstrup 2005), in which both low-and high-frequency glycinergic inputs generate inhibitory postsynaptic potentials (IPSPs) followed by rebound excitation (Sanchez et al 2008). The coincidence of these rebounds is hypothesized to be necessary for response facilitation (Fig.…”

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confidence: 99%

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Intracellular Recordings From Combination-Sensitive Neurons in the Inferior Colliculus

Peterson

Voytenko²,

Gans³

et al. 2008

Journal of Neurophysiology

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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.

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Section: Combination-sensitive Facilitatory Interactions May Occur Wimentioning

confidence: 79%

Section: R E S U L T Smentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Intracellular Recordings From Combination-Sensitive Neurons in the Inferior Colliculus

Peterson

Voytenko²,

Gans³

et al. 2008

Journal of Neurophysiology

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“…In addition to regions near the excitatory frequency response curve, tones at frequencies that are distant from the excitatory curve by an octave or more also decrease or facilitate excitatory responses (Mittman and Wenstrup 1995). These phenomena are simply inherited from lower auditory nuclei for many neurons (Portfors and Wenstrup 2001) but are influenced by the convergence of excitatory and inhibitory inputs within the IC for other neurons (Sanchez et al 2008). The effect of any serotonergic mechanism that regulated excitatory-inhibitory balance would therefore be likely to affect not only frequency tuning but also broader spectral sensitivity in the IC.…”

Section: Introductionmentioning

confidence: 99%

Serotonin 1B Receptor Modulates Frequency Response Curves and Spectral Integration in the Inferior Colliculus by Reducing GABAergic Inhibition

Hurley

Tracy²,

Bohorquez³

2008

Journal of Neurophysiology

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Hurley LM, Tracy JA, Bohorquez A. Serotonin 1B receptor modulates frequency response curves and spectral integration in the inferior colliculus by reducing GABAergic inhibition. J Neurophysiol 100: 1656 -1667, 2008. First published July 16, 2008 doi:10.1152/jn.90536.2008. The selectivity of sensory neurons for stimuli is often shaped by a balance between excitatory and inhibitory inputs, making this balance an effective target for regulation. In the inferior colliculus (IC), an auditory midbrain nucleus, the amplitude and selectivity of frequency response curves are altered by the neuromodulator serotonin, but the changes in excitatoryinhibitory balance that mediate this plasticity are not well understood. Previous findings suggest that the presynaptic 5-HT1B receptor may act to decrease the release of GABA onto IC neurons. Here, in vivo extracellular recording and iontophoresis of the selective 5-HT1B agonist CP93129 were used to characterize inhibition within and surrounding frequency response curves using two-tone protocols to indirectly measure inhibition as a decrease in spikes relative to an excitatory tone alone. The 5-HT1B agonist attenuated such two-tone spike reduction in a varied pattern among neurons, suggesting that the function of 5-HT1B modulation also varies. The hypothesis that the 5-HT1B receptor reduces inhibition was tested by comparing the effects of CP93129 and the GABA A antagonists bicuculline and gabazine in the same neurons. The effects of GABA A antagonists on spike count, tuning bandwidth, twotone ratio, and temporal response characteristics mimicked those of CP93129 across the neuron population. GABA A antagonists also blocked or reduced the facilitation of evoked responses by CP93129. These results are all consistent with the reduction of GABA A -mediated inhibition by 5-HT1B receptors in the IC, resulting in an increase in the level of evoked responses in some neurons, and a decrease in spectral selectivity in others. I N T R O D U C T I O NNeuromodulatory signals such as serotonin are broadly released in the brain in response to changes in internal state (Trulson andJacobs 1979, 1981) but transform the response properties of sensory neurons in highly specific ways (Hurley et al. 2004;Mooney et al. 1996;Xiang and Prince 2003). This specificity is achieved through the targeting of classes of neurons by a variety of receptor types that may alter intrinsic neuron properties or target presynaptic neurons and alter the release of neurotransmitter (Hoyer et al. 1994(Hoyer et al. , 2002. One consequence of these effects is that serotonin can alter the balance of different types of inputs within sensory regions. For example, serotonin may alter the balance between ascending versus descending projections (Mooney et al. 1996) or the balance between within-versus between-layer communication in the cortex (Xiang and Prince 2003).In the inferior colliculus (IC), an auditory midbrain nucleus, serotonin modifies a number of response properties, including both spectral and temporal aspects of ev...

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Developmental experience alters information coding in auditory midbrain and forebrain neurons

Woolley

Hauber

Theunissen

2010

Developmental Neurobiology

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In songbirds, species identity and developmental experience shape vocal behavior and behavioral responses to vocalizations. The interaction of species identity and developmental experience may also shape the coding properties of sensory neurons. We tested whether responses of auditory midbrain and forebrain neurons to songs differed between species and between groups of conspecific birds with different developmental exposure to song. We also compared responses of individual neurons to conspecific and heterospecific songs. Zebra and Bengalese finches that were raised and tutored by conspecific birds, and zebra finches that were cross-tutored by Bengalese finches were studied. Single-unit responses to zebra and Bengalese finch songs were recorded and analyzed by calculating mutual information, response reliability, mean spike rate, fluctuations in time-varying spike rate, distributions of time-varying spike rates, and neural discrimination of individual songs. Mutual information quantifies a response’s capacity to encode information about a stimulus. In midbrain and forebrain neurons, mutual information was significantly higher in normal zebra finch neurons than in Bengalese finch and cross-tutored zebra finch neurons, but not between Bengalese finch and cross-tutored zebra finch neurons. Information rate differences were largely due to spike rate differences. Mutual information did not differ between responses to conspecific and heterospecific songs. Therefore, neurons from normal zebra finches encoded more information about songs than did neurons from other birds, but conspecific and heterospecific songs were encoded equally. Neural discrimination of songs and mutual information were highly correlated. Results demonstrate that developmental exposure to vocalizations shapes the information coding properties of songbird auditory neurons.

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

Cited by 51 publications

References 41 publications

Intracellular Recordings From Combination-Sensitive Neurons in the Inferior Colliculus

Intracellular Recordings From Combination-Sensitive Neurons in the Inferior Colliculus

Serotonin 1B Receptor Modulates Frequency Response Curves and Spectral Integration in the Inferior Colliculus by Reducing GABAergic Inhibition

Developmental experience alters information coding in auditory midbrain and forebrain neurons

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