The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope

Middleton, Jason; Longtin, André; Benda, Jan; Maler, Leonard

doi:10.1073/pnas.0604103103

Cited by 100 publications

(124 citation statements)

References 48 publications

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“…If this coherence is equal to [C RR (f)] 1/2 at frequency f, then this implies that there was indeed a nonlinear relationship between the stimulus and response at frequency f and that we have uncovered its nature. Note that such approaches have been used previously with success (Middleton et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

“…Therefore, most analysis of these neurons has been performed using linear systems identification techniques (Wessel et al, 1996;Nelson et al, 1997;Kreiman et al, 2000). Recent results using information theoretic measures have confirmed the mostly linear response properties of P-units and no response to stimulus envelopes has been observed Kawasaki, 2006, 2008;Chacron, 2006;Middleton et al, 2006). These electroreceptor afferents make synaptic contact unto pyramidal cells within the electrosensory lateral line lobe (ELL) of the hindbrain.…”

mentioning

confidence: 99%

“…These electroreceptor afferents make synaptic contact unto pyramidal cells within the electrosensory lateral line lobe (ELL) of the hindbrain. In contrast to primary afferents, pyramidal cells show strong nonlinear coding (Chacron, 2006;Middleton et al, 2006), which is at least partly due to the fact that these cells respond to the stimulus waveform as well as its envelope (Middleton et al, 2006). An important caveat is that previous studies have characterized the responses of primary afferents to AM stimuli only up to a maximum temporal frequency of 256 Hz (Bastian, 1981a).…”

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confidence: 99%

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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%

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confidence: 99%

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confidence: 99%

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Neural heterogeneities influence envelope and temporal coding at the sensory periphery

Savard¹,

Krahe²,

Chacron³

2011

Neuroscience

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“…Animals were anaesthetized in 0.05% phenoxyethanol, and ELL tissue slices of 300-400 μm thickness were prepared, and recorded from, as previously described (Turner et al, 1994). For analysis of coherence or frequency content, RAMs were created as current injection protocols lasting 100 s, with frequency content between 0 and 60 Hz, as these frequencies are accurately represented in the pyramidal cell membrane voltage (Chacron et al, 2003a;Middleton et al, 2006). The current injections that we utilized are therefore a reasonable approximation of naturalistic sensory signals.…”

Section: In Vitro Electrophysiologymentioning

confidence: 99%

“…In vivo intracellular recordings (Chacron et al, 2005b;Middleton et al, 2006) have demonstrated that a pyramidal cell's membrane potential can faithfully track synaptically transmitted sensory input within a broad frequency range (0-60 Hz). The in vitro current injections are therefore a reasonable approximation of naturalistic sensory signals.…”

Section: Regulation Of Pyramidal Cell Burstingmentioning

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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Differential distribution of SK channel subtypes in the brain of the weakly electric fish Apteronotus leptorhynchus

Ellis

Maler

Dunn

2008

J of Comparative Neurology

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Calcium signals in vertebrate neurons can induce hyperpolarizing membrane responses through the activation of Ca(2+)-activated potassium channels. Of these, small conductance (SK) channels regulate neuronal responses through the generation of the medium after-hyperpolarization (mAHP). We have previously shown that an SK channel (AptSK2) contributes to signal processing in the electrosensory system of Apteronotus leptorhynchus. It was shown that for pyramidal neurons in the electrosensory lateral line lobe (ELL), AptSK2 expression selectively decreases responses to low-frequency signals. The localization of all the SK subunits throughout the brain of Apteronotus then became of substantial interest. We have now cloned two additional SK channel subunits from Apteronotus and determined the expression patterns of all three AptSK subunits throughout the brain. In situ hybridization experiments have revealed that, as in mammalian systems, the AptSK1 and 2 channels showed a partially overlapping expression pattern, whereas the AptSK3 channel was expressed in different brain areas. The AptSK1 and 2 channels were the primary subunits found in the major electrosensory processing areas. Immunohistochemistry further revealed distinct compartmentalization of the AptSK1 and 2 channels in the ELL. AptSK1 was localized to the apical dendrites of pyramidal neurons, whereas AptSK2 channels are primarily somatic. The distinct expression patterns of all three AptSK channels may reflect subtype-specific contributions to neuronal function, and the high homology between subtypes from a number of species suggests that the functional roles for each channel subtype are conserved from early vertebrate evolution.

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The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope

Cited by 100 publications

References 48 publications

Neural heterogeneities influence envelope and temporal coding at the sensory periphery

Neural heterogeneities influence envelope and temporal coding at the sensory periphery

Ionic and neuromodulatory regulation of burst discharge controls frequency tuning

Differential distribution of SK channel subtypes in the brain of the weakly electric fish Apteronotus leptorhynchus

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