Spike-Frequency Adaptation Separates Transient Communication Signals from Background Oscillations

Benda, Jan; Longtin, André; Maler, Len

doi:10.1523/jneurosci.4795-04.2005

Cited by 188 publications

(244 citation statements)

References 39 publications

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“…How nonrenewal spike train statistics affect correlated activity among neurons is an interesting topic that has been largely overlooked so far. For example, it is known that electroreceptor afferents in weakly electric fish that display negative ISI correlations can synchronize in response to transient high-frequency stimuli (Benda et al 2005(Benda et al , 2006Chacron et al 2005b), but do nonrenewal spike train statistics influence this synchronization and, if so, how? In general, further experimental and theoretical studies are needed to understand the effects of nonrenewal spike train statistics on population coding across systems.…”

Section: Nonrenewal Spike Train Statistics and Population Codingmentioning

confidence: 99%

Nonrenewal spike train statistics: causes and functional consequences on neural coding

Ávila-Ǻkerberg

Chacron

2011

Exp Brain Res

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Many neurons display significant patterning in their spike trains (e.g. oscillations, bursting), and there is accumulating evidence that information is contained in these patterns. In many cases, this patterning is caused by intrinsic mechanisms rather than external signals. In this review, we focus on spiking activity that displays nonrenewal statistics (i.e. memory that persists from one firing to the next). Such statistics are seen in both peripheral and central neurons and appear to be ubiquitous in the CNS. We review the principal mechanisms that can give rise to nonrenewal spike train statistics. These are separated into intrinsic mechanisms such as relative refractoriness and network mechanisms such as coupling with delayed inhibitory feedback. Next, we focus on the functional roles for nonrenewal spike train statistics. These can either increase or decrease information transmission. We also focus on how such statistics can give rise to an optimal integration timescale at which spike train variability is minimal and how this might be exploited by sensory systems to maximize the detection of weak signals. We finish by pointing out some interesting future directions for research in this area. In particular, we explore the interesting possibility that synaptic dynamics might be matched with the nonrenewal spiking statistics of presynaptic spike trains in order to further improve information transmission.

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Section: Nonrenewal Spike Train Statistics and Population Codingmentioning

confidence: 99%

Nonrenewal spike train statistics: causes and functional consequences on neural coding

Ávila-Ǻkerberg

Chacron

2011

Exp Brain Res

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“…Our results show that envelope responses can be generated already in the primary electroreceptor afferents. While it remains to be shown if ELL pyramidal neurons display envelope responses to the stimuli used in the present study, this is likely to be the case for two reasons: (1) primary afferents tend to display synchronous activity to high frequency stimuli (Benda et al, 2005; (2) ELL pyramidal neurons respond strongly to synchronous afferent activity (Bastian et al, 2002;Chacron et al, 2003a). As such, pyramidal cells may receive at least two streams of information about the time varying envelope: one through direct input from primary afferents and one through an inhibitory interneuron.…”

Section: Multiple Mechanisms For Generating An Envelope Response In Tmentioning

confidence: 90%

“…As such, they have traditionally been characterized using linear systems identification techniques (Scheich et al, 1973;Bastian, 1981a;Wessel et al, 1996;Kreiman et al, 2000;Benda et al, 2005). While the presence of static nonlinearities, such as rectification and saturation, has been shown previously, they were only described for constant-amplitude stimuli at intensities outside of the physiological range (Scheich et al, 1973).…”

Section: Nonlinear Coding In the Peripheral Electrosensory Systemmentioning

confidence: 99%

Neural heterogeneities influence envelope and temporal coding at the sensory periphery

Savard¹,

Krahe²,

Chacron³

2011

Neuroscience

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Peripheral sensory neurons respond to stimuli containing a wide range of spatio-temporal frequencies. We investigated electroreceptor neuron coding in the gymnotiform wave-type weakly electric fish Apteronotus leptorhynchus. Previous studies used low to mid temporal frequencies (<256 Hz) and showed that electroreceptor neuron responses to sensory stimuli could be almost exclusively accounted for by linear models, thereby implying a rate code. We instead used temporal frequencies up to 425 Hz, which is in the upper behaviorally relevant range for this species. We show that electroreceptors can: (A) respond up to the highest frequencies tested and (B) display strong nonlinearities in their responses to such stimuli. These nonlinearities were manifested by the fact that the responses to repeated presentations of the same stimulus were coherent at temporal frequencies outside of those contained in the stimulus waveform. Specifically, these consisted of low frequencies corresponding to the time varying contrast or envelope of the stimulus as well as higher harmonics of the frequencies contained in the stimulus. Heterogeneities in the afferent population influenced nonlinear coding as afferents with the lowest baseline firing rates tended to display the strongest nonlinear responses. To understand the link between afferent heterogeneity and nonlinear responsiveness, we used a phenomenological mathematical model of electrosensory afferents. Varying a single parameter in the model was sufficient to account for the variability seen in our experimental data and yielded a prediction: nonlinear responses to the envelope and at higher harmonics are both due to afferents with lower baseline firing rates displaying greater degrees of rectification in their responses. This prediction was verified experimentally as we found that the coherence between the half-wave rectified stimulus and the response resembled the coherence between the responses to repeated presentations of the stimulus in our dataset. This result shows that rectification cannot only give rise to responses to low frequency envelopes but also at frequencies that are higher than those contained in the stimulus. The latter result implies that information is contained in the fine temporal structure of electroreceptor afferent spike trains. Our results show that heterogeneities in peripheral neuronal populations can have dramatic consequences on the nature of the neural code.

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“…This requires tuning to AM frequencies ranging from ~1 to 300 Hz (Benda et al, 2005;Benda et al, 2006;Nelson and MacIver, 1999) and spatial frequencies of 0.2-2 cycles/cm (Nelson and MacIver, 1999). These AM frequencies have specific behavioural relevance, because prey cause only lowfrequency signals, whereas communication signals can extend to high frequencies.…”

Section: Pyramidal Cell Frequency Tuningmentioning

confidence: 99%

Ionic and neuromodulatory regulation of burst discharge controls frequency tuning

Mehaffey

Ellis

Krahe

et al. 2008

Journal of Physiology-Paris

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Sensory neurons encode natural stimuli by changes in firing rate or by generating specific firing patterns, such as bursts. Many neural computations rely on the fact that neurons can be tuned to specific stimulus frequencies. It is thus important to understand the mechanisms underlying frequency tuning. In the electrosensory system of the weakly electric fish, Apteronotus leptorhynchus, the primary processing of behaviourally relevant sensory signals occurs in pyramidal neurons of the electrosensory lateral line lobe (ELL). These cells encode low frequency prey stimuli with bursts of spikes and high frequency communication signals with single spikes. We describe here how bursting in pyramidal neurons can be regulated by intrinsic conductances in a cell subtype specific fashion across the sensory maps found within the ELL, thereby regulating their frequency tuning. Further, the neuromodulatory regulation of such conductances within individual cells and the consequences to frequency tuning are highlighted. Such alterations in the tuning of the pyramidal neurons may allow weakly electric fish to preferentially select for certain stimuli under various behaviourally relevant circumstances.

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Spike-Frequency Adaptation Separates Transient Communication Signals from Background Oscillations

Cited by 188 publications

References 39 publications

Nonrenewal spike train statistics: causes and functional consequences on neural coding

Nonrenewal spike train statistics: causes and functional consequences on neural coding

Neural heterogeneities influence envelope and temporal coding at the sensory periphery

Ionic and neuromodulatory regulation of burst discharge controls frequency tuning

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