Developmentally Regulated Rebound Depolarization Enhances Spike Timing Precision in Auditory Midbrain Neurons

Temporal sound cues are essential for sound recognition, pitch, rhythm, and timbre perception, yet how auditory neurons encode such cues is subject of ongoing debate. Rate coding theories propose that temporal sound features are represented by rate tuned modulation filters. However, overwhelming evidence also suggests that precise spike timing is an essential attribute of the neural code. Here we demonstrate that single neurons in the auditory midbrain employ a proportional code in which spike-timing precision and firing reliability covary with the sound envelope cues to provide an efficient representation of the stimulus. Spike-timing precision varied systematically with the timescale and shape of the sound envelope and yet was largely independent of the sound modulation frequency, a prominent cue for pitch. In contrast, spike-count reliability was strongly affected by the modulation frequency. Spike-timing precision extends from sub-millisecond for brief transient sounds up to tens of milliseconds for sounds with slow-varying envelope. Information theoretic analysis further confirms that spike-timing precision depends strongly on the sound envelope shape, while firing reliability was strongly affected by the sound modulation frequency. Both the information efficiency and total information were limited by the firing reliability and spike-timing precision in a manner that reflected the sound structure. This result supports a temporal coding strategy in the auditory midbrain where proportional changes in spike-timing precision and firing reliability can efficiently signal shape and periodicity temporal cues.

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Temperature-induced changes of spike timing precision and network synchronisation

BMC Neuroscience ◽

10.1186/1471-2202-16-s1-p219 ◽

2015 ◽

Vol 16 (S1) ◽

Author(s):

Jan-Hendrik Schleimer ◽

Janina Hesse ◽

Susanne Schreiber

Keyword(s):

Spike Timing ◽

Timing Precision ◽

Spike Timing Precision ◽

Induced Changes

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- Increases in Spike Timing Precision Improves Gustatory Discrimination upon Learning

Spike Timing ◽

10.1201/b14859-18 ◽

2013 ◽

pp. 340-361

Keyword(s):

Spike Timing ◽

Timing Precision ◽

Spike Timing Precision

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Analysis of the Spike Timing Precision in Retinal Ganglion Cells by the Stochastic Model

Frontiers in Neuroscience ◽

10.3389/conf.fnins.2010.13.00074 ◽

2010 ◽

Vol 4 ◽

Author(s):

Sakuragi Yuichiro

Keyword(s):

Stochastic Model ◽

Retinal Ganglion Cells ◽

Ganglion Cells ◽

Spike Timing ◽

Retinal Ganglion ◽

Timing Precision ◽

Spike Timing Precision

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Spike timing precision changes with spike rate adaptation in the owl's auditory space map

Journal of Neurophysiology ◽

10.1152/jn.00442.2015 ◽

2015 ◽

Vol 114 (4) ◽

pp. 2204-2219 ◽

Cited By ~ 2

Author(s):

Clifford H. Keller ◽

Terry T. Takahashi

Keyword(s):

Carrier Frequency ◽

Time Course ◽

Rate Adaptation ◽

Stimulus Level ◽

Spike Timing ◽

Spike Rate ◽

Temporal Precision ◽

Timing Precision ◽

Spike Timing Precision

Spike rate adaptation (SRA) is a continuing change of responsiveness to ongoing stimuli, which is ubiquitous across species and levels of sensory systems. Under SRA, auditory responses to constant stimuli change over time, relaxing toward a long-term rate often over multiple timescales. With more variable stimuli, SRA causes the dependence of spike rate on sound pressure level to shift toward the mean level of recent stimulus history. A model based on subtractive adaptation (Benda J, Hennig RM. J Comput Neurosci 24: 113–136, 2008) shows that changes in spike rate and level dependence are mechanistically linked. Space-specific neurons in the barn owl's midbrain, when recorded under ketamine-diazepam anesthesia, showed these classical characteristics of SRA, while at the same time exhibiting changes in spike timing precision. Abrupt level increases of sinusoidally amplitude-modulated (SAM) noise initially led to spiking at higher rates with lower temporal precision. Spike rate and precision relaxed toward their long-term values with a time course similar to SRA, results that were also replicated by the subtractive model. Stimuli whose amplitude modulations (AMs) were not synchronous across carrier frequency evoked spikes in response to stimulus envelopes of a particular shape, characterized by the spectrotemporal receptive field (STRF). Again, abrupt stimulus level changes initially disrupted the temporal precision of spiking, which then relaxed along with SRA. We suggest that shifts in latency associated with stimulus level changes may differ between carrier frequency bands and underlie decreased spike precision. Thus SRA is manifest not simply as a change in spike rate but also as a change in the temporal precision of spiking.

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Spike Timing Precision and Neural Error Correction: Local Behavior

Neural Computation ◽

10.1162/0899766053723069 ◽

2005 ◽

Vol 17 (7) ◽

pp. 1577-1601 ◽

Cited By ~ 7

Author(s):

Michael Stiber

Keyword(s):

Error Correction ◽

Dynamical Behavior ◽

Error Recovery ◽

Spike Timing ◽

Local Behavior ◽

Postsynaptic Spike ◽

Timing Precision ◽

Presynaptic Spike ◽

Spike Timing Precision ◽

High Degree

The effects of spike timing precision and dynamical behavior on error correction in spiking neurons were investigated. Stationary discharges—phase locked, quasiperiodic, or chaotic—were induced in a simulated neuron by presenting pacemaker presynaptic spike trains across a model of a prototypical inhibitory synapse. Reduced timing precision was modeled by jittering presynaptic spike times. Aftereffects of errors—in this communication, missed presynaptic spikes—were determined by comparing postsynaptic spike times between simulations identical except for the presence or absence of errors. Results show that the effects of an error vary greatly depending on the ongoing dynamical behavior. In the case of phase lockings, a high degree of presynaptic spike timing precision can provide significantly faster error recovery. For nonlocked behaviors, isolated missed spikes can have little or no discernible aftereffects (or even serve to paradoxically reduce uncertainty in postsynaptic spike timing), regardless of presynaptic imprecision. This suggests two possible categories of error correction: high-precision locking with rapid recovery and low-precision nonlocked with error immunity.

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