Adaptation Reduces Spike-Count Reliability, But Not Spike-Timing Precision, of Auditory Nerve Responses

Avissar, Michael; Furman, Adam C.; Saunders, James C.; Parsons, Thomas D.

doi:10.1523/jneurosci.5239-06.2007

Cited by 36 publications

(36 citation statements)

References 68 publications

(111 reference statements)

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“…3E; the population median as a function of level is shown in red). Similarly to what has been reported in various sensory systems (auditory system: Avissar et al 2007;Young and Barta 1986;other systems: Berry et al 1997;de Ruyter van Steveninck et al 1997), the TB responses exhibit sub-Poisson properties (FF Ͻ 1), that is, responses are more reproducible than for Poisson processes. The FF decreases as the stimulus level increases.…”

Section: Resultssupporting

confidence: 75%

Predicting spike timing in highly synchronous auditory neurons at different sound levels

Fontaine

Benichoux

Joris

et al. 2013

Journal of Neurophysiology

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Fontaine B, Benichoux V, Joris PX, Brette R. Predicting spike timing in highly synchronous auditory neurons at different sound levels. J Neurophysiol 110: 1672-1688, 2013. First published July 17, 2013 doi:10.1152/jn.00051.2013.-A challenge for sensory systems is to encode natural signals that vary in amplitude by orders of magnitude. The spike trains of neurons in the auditory system must represent the fine temporal structure of sounds despite a tremendous variation in sound level in natural environments. It has been shown in vitro that the transformation from dynamic signals into precise spike trains can be accurately captured by simple integrate-and-fire models. In this work, we show that the in vivo responses of cochlear nucleus bushy cells to sounds across a wide range of levels can be precisely predicted by deterministic integrate-and-fire models with adaptive spike threshold. Our model can predict both the spike timings and the firing rate in response to novel sounds, across a large input level range. A noisy version of the model accounts for the statistical structure of spike trains, including the reliability and temporal precision of responses. Spike threshold adaptation was critical to ensure that predictions remain accurate at different levels. These results confirm that simple integrate-and-fire models provide an accurate phenomenological account of spike train statistics and emphasize the functional relevance of spike threshold adaptation. bushy cell; level invariance; spike threshold adaptation; temporal coding TO LOCALIZE SOUND SOURCES in the horizontal plane, mammals rely mainly on interaural time differences (ITDs) at low frequencies. In cats, ITDs are smaller than 400 s (Tollin and Koka 2009) and behaviorally just noticeable differences in ITD can be as small as 20 s (Wakeford and Robinson

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Section: Resultssupporting

confidence: 75%

Predicting spike timing in highly synchronous auditory neurons at different sound levels

Fontaine

Benichoux

Joris

et al. 2013

Journal of Neurophysiology

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“…Similar results were reported for the locust's visual pathway (Gabbiani and Krapp, 2006) as well as for vertebrate visual (Sanchez-Vives et al, 2000a,b;Solomon et al, 2004), somatosensory (Derdikman et al, 2006, Katz et al, 2006 and auditory systems (McAlpine et al, 2000;McAlpine, 2004, 2005;Avissar et al, 2007). Different computational tasks may call for different distributions of adaptation mechanisms: e.g., (1) summation over many inputs to achieve high fidelity might require distributed mechanisms at several levels (Baccus and Meister, 2004;Baccus, 2006), whereas (2) converging inputs from different processing channels might require channelspecific adaptation mechanisms mostly at presynaptic stations (Abbott et al, 1997;Chance et al, 1998;Luksch et al, 2004).…”

Section: Functional Role Of the Distribution Of Adaptation Mechanismssupporting

confidence: 80%

The Origin of Adaptation in the Auditory Pathway of Locusts Is Specific to Cell Type and Function

Hildebrandt¹,

Benda²,

Hennig³

2009

J. Neurosci.

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We investigated the origin of spike frequency adaptation within a layered sensory network: the auditory pathway of locusts. Spike frequency adaptation as observed in an individual neuron may arise because of intrinsic or presynaptic adaptation mechanisms. To separate the contribution of different mechanisms, we recorded from the same cell during acoustic and intracellular current stimulation. We studied three identified neuron types that are representative for each network layer and participate in processing auditory patterns and localizing sound sources. By comparing current and acoustic stimulation, three distinct patterns of the distribution of adaptation mechanisms within the sensory network emerged: (1) balanced influence of both intrinsic and presynaptic adaptation mechanisms in an interneuron that summates over several receptor afferents (TN1), (2) predominantly inhibiting input as the source for spike frequency adaptation in a cell that transmits both pattern representation and directional information (BSN1), (3) primarily intrinsic, spiketriggered adaptation currents within an interneuron coding exclusively for direction (AN2). The time courses of spike frequency adaptation differed significantly between the cells types. Using the adaptation time constants, we were able to predict signal transmission properties for the different cells. We conclude that the adaptation mechanisms differ greatly among interneurons within this sensory pathway and are a function of their role in information processing.

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“…Details of the experiment and exclusion criteria for cells have been described previously (Avissar et al, 2007). Briefly, 3-to 24-dold White Leghorn chickens (Gallus domesticus) of either sex were surgically prepared for access to the cochlear nerve through the scala tympani.…”

Section: Methodsmentioning

confidence: 99%

“…At least 200 trials were presented to each cell and the occurrence times of spikes on each trial were stored on a hard disk with 10 s resolution. Cells were excluded if there were insufficient data, the health of the preparation was in question, or if the data did not pass a statistical stationarity test (Avissar et al, 2007). A total of 85 cells were included in the study.…”

Section: Methodsmentioning

confidence: 99%

“…Temporal coding of information is important in the auditory system, where neurons produce precisely timed spikes that synchronize and entrain to acoustic waves between 20 and 2000 Hz (Kiang, 1965;Rose et al, 1967;Joris et al, 1994;Köppl, 1997;Furman et al, 2006;Avissar et al, 2007). Both synchronization and entrainment by the auditory nerve are critical to sound encoding and are involved in the discrimination of pitch (Cariani, 1999), intensity (Colburn et al, 2003), and location (Carr and Konishi, 1988).…”

Section: Introductionmentioning

confidence: 99%

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Refractoriness Enhances Temporal Coding by Auditory Nerve Fibers

et al. 2013

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A universal property of spiking neurons is refractoriness, a transient decrease in discharge probability immediately following an action potential (spike). The refractory period lasts only one to a few milliseconds, but has the potential to affect temporal coding of acoustic stimuli by auditory neurons, which are capable of submillisecond spike-time precision. Here this possibility was investigated systematically by recording spike times from chicken auditory nerve fibers in vivo while stimulating with repeated pure tones at characteristic frequency. Refractory periods were tightly distributed, with a mean of 1.58 ms. A statistical model was developed to recapitulate each fiber's responses and then used to predict the effect of removing the refractory period on a cell-by-cell basis for two largely independent facets of temporal coding: faithful entrainment of interspike intervals to the stimulus frequency and precise synchronization of spike times to the stimulus phase. The ratio of the refractory period to the stimulus period predicted the impact of refractoriness on entrainment and synchronization. For ratios less than ϳ0.9, refractoriness enhanced entrainment and this enhancement was often accompanied by an increase in spike-time precision. At higher ratios, little or no change in entrainment or synchronization was observed. Given the tight distribution of refractory periods, the ability of refractoriness to improve temporal coding is restricted to neurons responding to low-frequency stimuli. Enhanced encoding of low frequencies likely affects sound localization and pitch perception in the auditory system, as well as perception in nonauditory sensory modalities, because all spiking neurons exhibit refractoriness.

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Adaptation Reduces Spike-Count Reliability, But Not Spike-Timing Precision, of Auditory Nerve Responses

Cited by 36 publications

References 68 publications

Predicting spike timing in highly synchronous auditory neurons at different sound levels

Predicting spike timing in highly synchronous auditory neurons at different sound levels

The Origin of Adaptation in the Auditory Pathway of Locusts Is Specific to Cell Type and Function

Refractoriness Enhances Temporal Coding by Auditory Nerve Fibers

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