Coding Properties of Two Classes of Afferent Nerve Fibers: High-Frequency Electroreceptors in the Electric Fish, Eigenmannia

Scheich, Henning; Bullock, Theodore H.; Hamstra, Robert H.

doi:10.1007/978-1-4684-9427-3_18

Cited by 34 publications

(73 citation statements)

References 14 publications

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“…These units are easily identified as their probability of firing increases with increasing EOD amplitude (Scheich et al, 1973). The recorded potential was amplified (Duo 773 Electrometer, World Precision Instruments, Sarasota, FL, USA), and digitized (10 kHz sampling rate) using CED 1401plus hardware and Spike2 software (Cambridge Electronic Design, Cambridge, UK).…”

Section: Recordingmentioning

confidence: 99%

“…In this study, we only consider AMs, because they represent the relevant stimulus for the P-type primary afferents (Scheich et al, 1973). As the electric organ of A. leptorhynchus consists of modified spinal motoneurons, it remains functional during the neuromuscular blockade used in the experiments.…”

Section: Stimulationmentioning

confidence: 99%

“…Electroreceptor afferents have traditionally been assumed to transmit information through a rate code as it was thought that their time dependent firing rate carried all the information about variations in EOD amplitude (Scheich et al, 1973;Bastian, 1981a,b;Gussin et al, 2007). 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).…”

Section: Nonlinear Coding In the Peripheral Electrosensory Systemmentioning

confidence: 99%

“…These distortions can be due to objects such as prey in their environment or to interference with the electric field of a conspecific. Here, we focus on the coding properties of P-type electroreceptor afferents in wavetype gymnotiform fish whose probability of firing an action potential on a given EOD cycle depends on the amplitude of the EOD, that is, they respond to amplitude modulations (AMs) of the EOD through smooth changes in firing rate (Scheich et al, 1973;Bastian, 1981a). Static nonlinearities, such as saturation and rectification, have been described for these P-units but only for stimulus intensities that are outside those found in behaviorally relevant situations (Scheich et al, 1973).…”

mentioning

confidence: 99%

“…Here, we focus on the coding properties of P-type electroreceptor afferents in wavetype gymnotiform fish whose probability of firing an action potential on a given EOD cycle depends on the amplitude of the EOD, that is, they respond to amplitude modulations (AMs) of the EOD through smooth changes in firing rate (Scheich et al, 1973;Bastian, 1981a). Static nonlinearities, such as saturation and rectification, have been described for these P-units but only for stimulus intensities that are outside those found in behaviorally relevant situations (Scheich et al, 1973). 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).…”

mentioning

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: Recordingmentioning

confidence: 99%

Section: Stimulationmentioning

confidence: 99%

Section: Nonlinear Coding In the Peripheral Electrosensory Systemmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

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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Localization of nicotinamide adenine dinucleotide phosphate‐diaphorase activity in electrosensory and electromotor systems of a gymnotiform teleost, Apteronotus leptorhynchus

Turner

Moroz

1995

J of Comparative Neurology

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The distribution of nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d) activity was determined in electrosensory and electromotor systems of the weakly electric gymnotiform teleost Apteronotus leptorhynchus as an indicator of putative nitric oxide synthase-containing cells. NADPH-d activity was detected in electroreceptors and in afferent nerves of both ampullary and type I and type II tuberous organs. All cell bodies within the anterior lateral line nerve ganglion were positive for NADPH-d activity, as were the primary afferent axons and termination fields in the medullary electrosensory lateral line lobe. In the corpus cerebelli and valvula cerebelli, NADPH-d label was present in Purkinje cell somata, mossy fiber synaptic glomeruli, granule cells, and parallel fibers. In the midbrain, NADPH-d activity was apparent in layer VIIIB of the torus semicircularis dorsalis and in electrosensory laminae of the optic tectum. NADPH-d was particularly associated with diencephalic electrosensory and electromotor nuclei, including the prepacemaker nucleus, the nucleus subelectrosensorius, and the central posterior nucleus of the thalamus. Intense NADPH-d activity was present in pacemaker and relay cells of the medullary pacemaker nucleus but was absent from a novel class of smaller cells in this structure. Relay cell axons and spinal electromotor neurons and their axons within the electric organ were positive for NADPH-d activity. These results indicate that putative nitric oxide synthase-containing neurons in Apteronotus are localized preferentially to electrosensory and electromotor structures, suggesting a role for nitric oxide in determining the activity of cells involved in detecting or generating weakly electric fields.

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Motion processing across multiple topographic maps in the electrosensory system

Khosravi‐Hashemi

Chacron

2014

Physiol Rep

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Animals can efficiently process sensory stimuli whose attributes vary over orders of magnitude by devoting specific neural pathways to process specific features in parallel. Weakly electric fish offer an attractive model system as electrosensory pyramidal neurons responding to amplitude modulations of their self‐generated electric field are organized into three parallel maps of the body surface. While previous studies have shown that these fish use parallel pathways to process stationary stimuli, whether a similar strategy is used to process motion stimuli remains unknown to this day. We recorded from electrosensory pyramidal neurons in the weakly electric fish Apteronotus leptorhynchus across parallel maps of the body surface (centromedial, centrolateral, and lateral) in response to objects moving at velocities spanning the natural range. Contrary to previous observations made with stationary stimuli, we found that all cells responded in a similar fashion to moving objects. Indeed, all cells showed a stronger directionally nonselective response when the object moved at a larger velocity. In order to explain these results, we built a mathematical model incorporating the known antagonistic center–surround receptive field organization of these neurons. We found that this simple model could quantitatively account for our experimentally observed differences seen across E and I‐type cells across all three maps. Our results thus provide strong evidence against the hypothesis that weakly electric fish use parallel neural pathways to process motion stimuli and we discuss their implications for sensory processing in general.

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Coding Properties of Two Classes of Afferent Nerve Fibers: High-Frequency Electroreceptors in the Electric Fish, Eigenmannia

Cited by 34 publications

References 14 publications

Neural heterogeneities influence envelope and temporal coding at the sensory periphery

Neural heterogeneities influence envelope and temporal coding at the sensory periphery

Localization of nicotinamide adenine dinucleotide phosphate‐diaphorase activity in electrosensory and electromotor systems of a gymnotiform teleost, Apteronotus leptorhynchus

Motion processing across multiple topographic maps in the electrosensory system

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