Fractal noise strength in auditory-nerve fiber recordings

Kelly, O.E.; Johnson, Don H.; Delgutte, Bertrand; Cariani, Peter

doi:10.1121/1.415409

Cited by 24 publications

(20 citation statements)

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“…Discharge patterns recorded from a variety of sensory systems, including auditory nerve, exhibit predominantly sub-Poisson statistics manifest by FFs less than one for time windows on the order of tens of milliseconds, suggesting reliable, nonrandom spike discharges (Teich and Khanna, 1985;Young and Barta, 1986;Berry et al, 1997;de Ruyter van Steveninck et al, 1997;DeWeese et al, 2003;Schaette et al, 2005). This is in contrast to the predominantly supra-Poisson statistics observed with longer counting windows (Teich et al, 1990;Lowen and Teich, 1992;Kelly et al, 1996). Over the counting window analyzed in this study, all auditory nerve fibers responded with sub-Poisson spike-count reliability (Figs.…”

Section: Spike-count Reliabilitycontrasting

confidence: 52%

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

Avissar¹,

Furman²,

Saunders³

et al. 2007

Journal of Neuroscience

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Sensory systems use adaptive coding mechanisms to filter redundant information from the environment to efficiently represent the external world. One such mechanism found in most sensory neurons is rate adaptation, defined as a reduction in firing rate in response to a constant stimulus. In auditory nerve, this form of adaptation is likely mediated by exhaustion of release-ready synaptic vesicles in the cochlear hair cell. To better understand how specific synaptic mechanisms limit neural coding strategies, we examined the trial-to-trial variability of auditory nerve responses during short-term rate-adaptation by measuring spike-timing precision and spike-count reliability. After adaptation, precision remained unchanged, whereas for all but the lowest-frequency fibers, reliability decreased. Modeling statistical properties of the hair cell-afferent fiber synapse suggested that the ability of one or a few vesicles to elicit an action potential reduces the inherent response variability expected from quantal neurotransmitter release, and thereby confers the observed count reliability at sound onset. However, with adaptation, depletion of the readily releasable pool of vesicles diminishes quantal content and antagonizes the postsynaptic enhancement of reliability. These findings imply that during the course of short-term adaptation, coding strategies that employ a rate code are constrained by increased neural noise because of vesicle depletion, whereas those that employ a temporal code are not.

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Section: Spike-count Reliabilitycontrasting

confidence: 52%

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

Avissar¹,

Furman²,

Saunders³

et al. 2007

Journal of Neuroscience

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“…Long-term correlations and fractal behavior have been observed in patterns of action potential firings recorded in a variety of neuronal preparations including the auditory system (Kelly et al, 1996;Kumar and Johnson, 1993;Lowen and Teich, 1996;Powers and Salvi, 1992;Teich 1989), visual system Turcott et al, 1995), somatosensory cortex (Wise, 1981), mesencephalic reticular formation (Grüneis et al, 1993), neocortex (Linkenkaer-Hansen et al, 2001, 2004, and medulla (Lewis et al, 2001). Although a few studies have reported the lack of the fractal behavior in neural systems like the primary vestibule of the auditory system (Teich, 1989), the presence of the fractal behavior throughout various brain regions suggests that the fractal behavior found in SCN neurons is a general feature of neurons, rather than a specific one pertaining to the SCN.…”

Section: Discussionmentioning

confidence: 99%

Fractal Stochastic Modeling of Spiking Activity in Suprachiasmatic Nucleus Neurons

et al. 2005

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Individual neurons in the suprachiasmatic nucleus (SCN), the master biological clock in mammals, autonomously produce highly complex patterns of spikes. We have shown that most (approximately 90%) SCN neurons exhibit truly stochastic interspike interval (ISI) patterns. The aim of this study was to understand the stochastic nature of the firing patterns in SCN neurons by analyzing the ISI sequences of 150 SCN neurons in hypothalamic slices. Fractal analysis, using the periodogram, Fano factor, and Allan factor, revealed the presence of a 1/f-type power-law (fractal) behavior in the ISI sequences. This fractal nature was persistent after the application of the GABAA receptor antagonist bicuculline, suggesting that the fractal stochastic activity is an intrinsic property of individual SCN neurons. Based on these physiological findings, we developed a computational model for the stochastic SCN neurons to find that their stochastic spiking activity was best described by a gamma point process whose mean firing rate was modulated by a fractal binomial noise. Taken together, we suggest that SCN neurons generate temporal spiking patterns using the fractal stochastic point process.

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“…Examples include the openings and closings of ion channels (Läuger, 1988;Millhauser et al, 1988;Liebovitch and Tóth, 1990;Teich et al, 1991;Lowen and Teich, 1993a-c); patterns of action-potential firings in the auditory system (Teich, 1989(Teich, , 1992Teich et al, 1990;Powers and Salvi, 1992;Kumar and Johnson, 1993;Kelly et al, 1996;Lowen and Teich, 1996), visual system (Turcott et al, 1995Teich et al, 1996aTeich et al, ,b, 1997, somatosensory cortex (Wise, 1981), and mesencephalic reticular formation (Grüneis et al, 1993); and even the sequence of human heartbeats (Kobayashi and Musha, 1982;Saul et al, 1988;Turcott andTeich, 1993, 1996). In almost all of these cases, the upper limit of the observed time over which fractal correlations exist is imposed by the duration of the recording.…”

Section: Discussionmentioning

confidence: 99%

Quantal Neurotransmitter Secretion Rate Exhibits Fractal Behavior

et al. 1997

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The rate of exocytic events from both neurons and nonneuronal cells exhibits fluctuations consistent with fractal (selfsimilar) behavior in time, as evidenced by a number of statistical measures. We explicitly demonstrate this for neurotransmitter secretion at Xenopus neuromuscular junctions and for rat hippocampal synapses in culture; the exocytosis of exogenously supplied neurotransmitter from cultured Xenopus myocytes and from rat fibroblasts behaves similarly. The magnitude of the fluctuations of the rate of exocytic events about the mean decreases slowly as the rate is computed over longer and longer time periods, the periodogram decreases in power-law manner with frequency, and the Allan factor (relative variance of the number of exocytic events) increases as a power-law function of the counting time. These features are hallmarks of self-similar behavior. Their description requires models that exhibit long-range correlation (memory) in event occurrences. We have developed a physiologically plausible model that accords with all of the statistical measures that we have examined. The appearance of fractal behavior at synapses, as well as in systems comprising collections of synapses, indicates that such behavior is ubiquitous in neural signaling. Key words: quantal secretion; vesicular exocytosis; miniature endplate currents; fractal; long-term correlation; lognormal process; Xenopus neuromuscular junction; myocyte autoreception; fibroblast; hippocampal synapseCommunication in the nervous system is mediated by actionpotential-initiated exocytosis of multiple vesicular packets (quanta) of neurotransmitter (Katz, 1966). Even in the absence of such action potentials, however, many neurons spontaneously release individual packets of neurotransmitter (Fatt and Katz, 1952). A packet may contain from 7000 to 10,000 molecules of acetylcholine (ACh), if we use the neuromuscular junction as an example (Kuffler and Yoshikami, 1975). On arrival at the postsynaptic membrane, the ACh molecules induce elementary endplate currents (EEC s), which take the form of nonstationary two-(or multi-) state on -off sequences (Sakmann, 1992). Current flows when the ACh channel is open (i.e., when its two binding sites are occupied by agonist) and ceases when the channel is closed. A postsynaptic miniature endplate current (M EPC) comprises some 1000 EEC s (Sakmann, 1992). It was shown by Del Castillo and Katz (1954) that superpositions of M EPC -like events comprise the postsynaptic endplate currents elicited by nerve impulses.It generally has been assumed that the sequence of MEPCs forms a memoryless stochastic process (Fatt and Katz, 1952). However, Rotshenker and Rahamimoff (1970) discovered that exocytosis in the frog neuromuscular junction can exhibit correlation (memory) over a period of seconds, provided that extracellular C a 2ϩ levels are elevated above their normal values. Cohen et al. (1974b) subsequently found such correlation (event clustering) even in the absence of elevated Ca 2ϩ levels. In this paper we study the statis...

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Fractal noise strength in auditory-nerve fiber recordings

Cited by 24 publications

References 0 publications

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

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

Fractal Stochastic Modeling of Spiking Activity in Suprachiasmatic Nucleus Neurons

Quantal Neurotransmitter Secretion Rate Exhibits Fractal Behavior

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