Response properties of electrosensory units in the midbrain tectum of the paddlefish (<i>Polyodon spathula</i> Walbaum)

Hofmann, Michaël; Jung, Sarah Nicola; Siebenaller, U; Preissner, M; Chagnaud, Boris P.; Wilkens, Lon A.

doi:10.1242/jeb.009795

Cited by 7 publications

(5 citation statements)

References 22 publications

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“…70 Interestingly, a wide uniform frequency response was reported for higher-level electrosensory neurons in the paddlefish brain. 19,35 They, unlike primary afferents characteristically show low background firing rates and thus may work as rectifiers, which are a canonical example of a nonlinear decoder.…”

Section: Linear and Non-linear Responses And Codingmentioning

confidence: 99%

Sensory coding in oscillatory electroreceptors of paddlefish

Neiman

Russell²

2011

Chaos: An Interdisciplinary Journal of Nonlinear Science

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Coherence and information theoretic analyses were applied to quantitate the response properties and the encoding of time-varying stimuli in paddlefish electroreceptors (ERs), studied in vivo. External electrical stimuli were Gaussian noise waveforms of varied frequency band and strength, including naturalistic waveforms derived from zooplankton prey. Our coherence analyses elucidated the role of internal oscillations and transduction processes in shaping the 0.5-20 Hz best frequency tuning of these electroreceptors, to match the electrical signals emitted by zooplankton prey. Stimulus-response coherence fell off above approximately 20 Hz, apparently due to intrinsic limits of transduction, but was detectable up to 40-50 Hz. Aligned with this upper fall off was a narrow band of intense internal noise at $25 Hz, due to prominent membrane potential oscillations in cells of sensory epithelia, which caused a narrow deadband of external insensitivity. Using coherence analysis, we showed that more than 76% of naturalistic stimuli of weak strength, $1 lV=cm, was linearly encoded into an afferent spike train, which transmitted information at a rate of $30 bits=s. Stimulus transfer to afferent spike timing became essentially nonlinear as the stimulus strength was increased to induce bursting firing. Strong stimuli, as from nearby zooplankton prey, acted to synchronize the bursting responses of afferents, including across populations of electroreceptors, providing a plausible mechanism for reliable information transfer to higher-order neurons through noisy synapses. Rhythmical activity underlies various complex physiological processes in central nervous systems. Peripheral sensory receptors, on the other hand, are often considered as "passive" systems with relatively simple and linear dynamics. Nevertheless, self-sustained oscillations have been observed in several types of peripheral sensory receptors. This paper reports on stimulus encoding in electroreceptors (ERs) of paddlefish, which use passive electrosense to feed on zooplankton. A single peripheral electroreceptor in paddlefish is a complex system comprised of several thousands of sensory epithelial cells innervated by a few primary sensory neurons (afferents). It embeds distinct oscillators: one resides in a population of epithelial cells, synaptically coupled to another oscillator in afferent terminals. In contrast to auditory receptors, which resonate to sound waves of certain frequency, neither epithelial nor afferent rhythms of electroreceptors match the low-frequency bioelectric signals emitted by zooplankton prey. We applied Gaussian noise stimuli to study how oscillators embedded in paddlefish electroreceptors shape the linear and nonlinear responses of electroreceptors, and to characterize quantitatively how external stimuli, including bioelectrical signals from zooplankton prey, are encoded into the timing of afferent firing.

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Section: Linear and Non-linear Responses And Codingmentioning

confidence: 99%

Sensory coding in oscillatory electroreceptors of paddlefish

Neiman

Russell²

2011

Chaos: An Interdisciplinary Journal of Nonlinear Science

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“…However, the dipole source was placed under the ventral rostrum of sturgeon, thus the condition was different from that in the previous study of paddlefish [17] . It is clear that this response of inhibition and excitation may be used in prey detection by sturgeon.…”

Section: Different Responses In Paddlefish and Sturgeonmentioning

confidence: 98%

“…This suggests that the spontaneous rate acts as a carrier frequency in electrosensory information-processing. Carrier modulation also occurs in paddlefish, and the highest stimulus frequency must be lower than the mean rate to allow accurate coding in the signal bandwidth [17] . Thus, the neurons with high spontaneous activity had the highest relative evoked rates during the stimulus.…”

Section: Electrosensory Information-processing Related Tomentioning

confidence: 99%

“…In catfish, two populations of cells with opposite response polarity were described in their lateral line lobes (equivalent to the DON) [16] . In paddlefish, neurons with opposite phase-locking relationships were found with the same stimulus, and may receive different information from fibers innervating the rostrum and gill cover [17] .…”

Section: Different Responses In Paddlefish and Sturgeonmentioning

confidence: 99%

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Response properties of the electrosensory neurons in hindbrain of the white sturgeon, Acipenser transmontanus

et al. 2011

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ObjectiveThe passive electrosense is a primitive sensory modality in the Chondrostei, which include sturgeon and paddlefish. Using electroreceptors, these fish detect the weak electric fields from other animals or geoelectric sources, and use this information for prey detection or other behaviors. The primary afferent fibers innervating the electroreceptors project to a single hindbrain target called the dorsal octavolateral nucleus (DON), where the electrosensory information is first processed. Here, we investigated the electrophysiological properties of DON neurons. Methods Extracellular recording was used to investigate the response properties of DON neurons to dipole electric fields with different amplitudes and frequencies in the white sturgeon, Acipenser transmontanus. Results The DON neurons showed regular spontaneous activity and could be classified into two types: neurons with a low spontaneous rate (<10 Hz) and those with a high spontaneous rate (>10 Hz). In response to sinusoidal electric field stimuli, DON neurons showed sinusoidally-modulated and phase-locked firing. In addition, neurons showed opposite phase responses corresponding to the different directions of the dipole. Conclusion The response properties of DON neurons match the electrosensory biological function in sturgeon, as they match the characteristics of the electric fields of its prey.

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“…Electroreception is therefore an important aspect of the ecology of all aquatic animals, whether they are the hunters or the hunted, and we still make new discoveries today in an attempt to fully understand this sense in vertebrates [e.g. neurobiology (Hofmann et al, 2008); evolution (Zakon et al, 2008); field description (Babineau et al, 2006)]. …”

Section: Introductionmentioning

confidence: 99%

Making sense of electrical sense in crayfish

Patullo

Macmillan

2010

Journal of Experimental Biology

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SUMMARYThe five sensory modalities of humans are also found in a wide range of invertebrates. Other vertebrates have evolved additional special senses, such as the magnetic sense, which are also found in some invertebrates. However, there remain a few sensory abilities that curiously appear to be found in either vertebrates or invertebrates, but not both. For example, electrosensitivity -the ability to detect electric fields in water -which should benefit vertebrates and invertebrates alike, is apparently only used by vertebrates. However, recent reports suggest that some invertebrates could have an electric sense. Here we examine that possibility further and demonstrate a behavioural threshold to low-level electrical fields in two freshwater invertebrates. The responses are not low enough for them to detect the Earth's magnetic field as some other electroreceptive species can do, but sufficiently low for them to use in navigation or prey and predator detection. This finding challenges the current view of the sensory world of aquatic invertebrates and has implications for the evolution of this ability.

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Response properties of electrosensory units in the midbrain tectum of the paddlefish (Polyodon spathula Walbaum)

Abstract: SUMMARY

Cited by 7 publications

References 22 publications

Sensory coding in oscillatory electroreceptors of paddlefish

Sensory coding in oscillatory electroreceptors of paddlefish

Response properties of the electrosensory neurons in hindbrain of the white sturgeon, Acipenser transmontanus

Making sense of electrical sense in crayfish

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