An improved method for the estimation of firing rate dynamics using an optimal digital filter

Cherif, Sofiane; Cullen, Kathleen E.; Galiana, Henrietta L.

doi:10.1016/j.jneumeth.2008.05.021

Cited by 40 publications

(34 citation statements)

References 30 publications

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“…The response R(t) was first filtered using a 15 point Kaiser filter in order to obtain the time dependent firing rate. Previous studies have shown that such a filter provides a good estimate of modulations in the time varying firing rate of neurons provided that the mean firing rate is high (Cherif et al, 2008), which is the case here as primary afferents have firing rates greater than 150 Hz (Gussin et al, 2007). The stimulus waveform S(t) was aligned to the time dependent firing rate and transformed according to:…”

Section: Discussionmentioning

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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Section: Discussionmentioning

confidence: 99%

Neural heterogeneities influence envelope and temporal coding at the sensory periphery

Savard¹,

Krahe²,

Chacron³

2011

Neuroscience

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“…Head acceleration signals were digitally filtered at 20 Hz. The neural discharge was represented using a spike density function in which a Kaiser window was convolved with the spike train (Cherif et al 2008). The resting discharge of each unit (defined as the mean firing rate when stationary with the head in the stereotaxic position) and CV of the interspike interval were determined.…”

Section: Discussionmentioning

confidence: 99%

Response of Vestibular Nerve Afferents Innervating Utricle and Saccule During Passive and Active Translations

Jamali

Sadeghi

Cullen

2009

Journal of Neurophysiology

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Jamali M, Sadeghi SG, Cullen KE. Response of vestibular-nerve afferents innervating utricle and saccule during passive and active translations. J Neurophysiol 101: 141-149, 2009. First published October 29, 2008 doi:10.1152/jn.91066.2008. The distinction between sensory inputs that are a consequence of our own actions from those that result from changes in the external world is essential for perceptual stability and accurate motor control. In this study, we investigated whether linear translations are encoded similarly during active and passive translations by the otolith system. Vestibular nerve afferents innervating the saccule or utricle were recorded in alert macaques. Single unit responses were compared during passive whole body, passive head-on-body, and active head-on-body translations (vertical, fore-aft, or lateral) to assess the relative influence of neck proprioceptive and efference copy-related signals on translational coding. The response dynamics of utricular and saccular afferents were comparable and similarly encoded head translation during passive whole body versus head-on-body translations. Furthermore, when monkeys produced active head-on-body translations with comparable dynamics, the responses of both regular and irregular afferents remained comparable to those recorded during passive movements. Our findings refute the proposal that neck proprioceptive and/or efference copy inputs coded by the efferent system function to modulate the responses of the otolith afferents during active movements. We conclude that the vestibular periphery provides faithful information about linear movements of the head in the space coordinates, regardless of whether they are self-or externally generated.

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“…Notably, it has been shown that Kaiser filters consistently outperformed currently used methods, such as reciprocal ISI (and also spike density function and rate histogram) particularly at higher frequencies, as characterized by minimal aliasing, phase, and amplitude distortion (Cherif et al, 2008). Thus, using a Kaiser filter gives rise to lower threshold values than other techniques (Yu et al, 2012).…”

Section: Analysis Of Neuronal Dischargesmentioning

confidence: 99%

“…The value of bin j was set to 1 if it contained an action potential and 0 otherwise as described previously (Sadeghi et al, 2007). Then, fr(t) was obtained by convolving the spike train r(t) with a Kaiser window whose cutoff frequency was set to 0.1 Hz above the stimulus frequency to ensure that the pass band of the filter includes the frequency of the stimulus (Cherif et al, 2008;Jamali et al, 2009;Yu et al, 2012). Alternatively, we estimated the time-dependent firing rate fr ISI (t) as the reciprocal of the ISI as described previously (Yu et al, 2012).…”

Section: Analysis Of Neuronal Dischargesmentioning

confidence: 99%

“…At the earliest stages of vestibular processing, otolith afferents detect linear acceleration. Studies performed in other systems show that central pathways must integrate information transmitted by peripheral sensory neuron populations to explain perceptual thresholds as peripheral sensory neurons display much higher values (visual: Pelli, 1985;Amano et al, 2006; Shadlen et al, 1996; auditory: Pfingst and Xu, 2004;Bizley et al, 2010; cross modal: McDonald et al, 2000; Shams et al, 2000 Shams et al, , 2002 vestibular (rotation): Sadeghi et al, 2007;Massot et al, 2011). Surprisingly, however, Yu et al (2012) recently extrapolated threshold values for single macaque otolith afferents that were comparable with perceptual ones, which suggests that the vestibular system uses a unique strategy for coding linear acceleration.…”

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confidence: 99%

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Strong Correlations between Sensitivity and Variability Give Rise to Constant Discrimination Thresholds across the Otolith Afferent Population

Jamali

Carriot

Chacron

et al. 2013

Journal of Neuroscience

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The vestibular system is vital for our sense of linear self-motion. At the earliest processing stages, the otolith afferents of the vestibular nerve encode linear motion. Their resting discharge regularity has long been known to span a wide range, suggesting an important role in sensory coding, yet to date, the question of how this regularity alters the coding of translational motion is not fully understood. Here, we recorded from single otolith afferents in macaque monkeys during linear motion along the preferred directional axis of each afferent over a wide range of frequencies (0.5-16 Hz) corresponding to physiologically relevant stimulation. We used signal-detection theory to directly measure neuronal thresholds and found that values for single afferents were substantially higher than those observed for human perception even when a Kaiser filter was used to provide an estimate of firing rate. Surprisingly, we further found that neuronal thresholds were independent of both stimulus frequency and resting discharge regularity. This was because increases in trial-to-trial variability were matched by increases in sensitivity such that their ratio remains constant: a coding strategy that markedly differs from that used by semicircular canal vestibular afferents to encode rotations. Finally, using Fisher information, we show that pooling the activities of multiple otolith afferents gives rise to neural thresholds comparable with those measured for perception. Together, our results strongly suggest that higher-order structures integrate inputs across afferent populations to provide our sense of linear motion and provide unexpected insight into the influence of variability on sensory encoding. IntroductionAs we navigate through the world, our brain integrates information originating from the vestibular, visual, and proprioceptive systems to compute an estimate of self-motion. However, vestibular contributions to motion perception have been difficult to study because the pathways are inherently multisensory. Numerous studies have attempted to quantify perceptual vestibular thresholds for linear motion in humans (Walsh, 1961(Walsh, , 1962 Young and Meiry, 1968;Jones and Young, 1978; Benson et al., 1986; Zupan and Merfeld, 2008; MacNeilage et al., 2010a,b;Naseri and Grant, 2012). Notably, recent results show that vestibular cues play a central role in determining perceptual thresholds and further suggest that they can be as low as ϳ1.5 cm/s 2 (Valko et al., 2012). To date, the neural mechanisms that give rise to our sense of linear self-motion are essentially unknown. At the earliest stages of vestibular processing, otolith afferents detect linear acceleration. Studies performed in other systems show that central pathways must integrate information transmitted by peripheral sensory neuron populations to explain perceptual thresholds as peripheral sensory neurons display much higher values (visual: Pelli, 1985;Amano et al., 2006; Shadlen et al., 1996; auditory: Pfingst and Xu, 2004;Bizley et al., 2010; cross modal: ...

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An improved method for the estimation of firing rate dynamics using an optimal digital filter

Cited by 40 publications

References 30 publications

Neural heterogeneities influence envelope and temporal coding at the sensory periphery

Neural heterogeneities influence envelope and temporal coding at the sensory periphery

Response of Vestibular Nerve Afferents Innervating Utricle and Saccule During Passive and Active Translations

Strong Correlations between Sensitivity and Variability Give Rise to Constant Discrimination Thresholds across the Otolith Afferent Population

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