Neurosci Bull December 1, 2011, 27(6): 422–429. http://www.neurosci.cnDOI: 10.1007/s12264-011-1635-y422

·Original Article·

Corresponding author: Jiakun SongTel: +86-21-61900455E-mail: jksong@shou.edu.cnArticle ID: 1673-7067(2011)06-0422-08Received date: 2011-06-27; Accepted date: 2011-08-31

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

Xuguang Zhang1, Hendrik Herzog2, Jiakun Song1, Xiaojie Wang1, Chunxin Fan1, Hongyi Guo1

1Shanghai Ocean University, Institute for Marine Biosystems and Neuroscience, Shanghai 201306, China 2Institute of Zoology, University of Bonn, Bonn 53115, Germany

© Shanghai Institutes for Biological Sciences, CAS and Springer-Verlag Berlin Heidelberg 2011

Abstract: Objective The 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 re-cording 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 spon-taneous 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.

Keywords: electrosense; sturgeon; dipole; single unit; hindbrain

1 Introduction

Sensing low-frequency weak electric fields is a primi-tive sense of organisms as old as the ancestor to both jawed and jawless vertebrates[1]. This sense is important for prey detection, mating and orientation in almost all electrosen-sory fishes[2]. The electrosense was passed down to major taxa of living aquatic vertebrates[3]. It has been lost in most modern teleost fish, but still exists in some and can be cat-egorized into active or passive electrosense[4].

The sturgeon and paddlefish are sister groups of primi-tive Chondrostei and are well known as passive electrosen-sory fishes[3]. The biological function of the electrosensory system in prey detection has been well documented in both[5]. The dermal electroreceptor has also been described in stur-geon and paddlefish[6,7], and the processing of electrosensory information in paddlefish has been elucidated[8,9]. However, due to the differences in body type and feeding habits, the mechanism of electrosensory processing in sturgeon re-mains unknown.

In all passive electrosensory fish, the primary afferent fibers innervating the electroreceptors project to a single hindbrain area, the dorsal octavolateral nucleus (DON), which in turn projects to various targets in the midbrain[10].

Xuguang Zhang et al. Response properties of the electrosensory neurons in hindbrain of the white sturgeon, Acipenser transmontanus 423

It is of special interest to compare the initial electrosen-sory information processing of sturgeon with that of other electrosensory fishes. There have been some physiological studies of the DON in non-teleost and teleost fishes[8,11,12]. However, the response characteristics of the DON in stur-geon remain to be determined. The present study aimed to characterize the response properties of the DON in the white sturgeon, Acipenser transmontanus, to local dipolar sinusoidal fields of different frequencies, amplitudes and directions of polarity.

2 Materials and methods

2.1 Animals Twelve white sturgeon ranging from 10 to 15 cm in length, were obtained from a local fish hatchery in Bonn, Germany in December, 2010. They were kept in a concrete tank of approximately 500 L, filled with bio-filtered and aerated dechlorinated tap water. Before surgery, the fish was anesthetized by immersion in MS-222 (1:10 000, v/v) for 3–5 min, and then immobilized by injection of 20–30 μL pan-curonium bromide (Organon Teknika, Oberschleissheim, Germany) into the back muscles. Afterwards, the skull was opened to expose the DON. The fish was mounted on a custom-made fixation plate in the recording tank and the gills were irrigated with fresh water through the mouth.2.2 Stimulation The fish were first placed in a quasi-uniform electric field, which was produced by two metal plates perpendicular to the rostro-caudal axis, one 15 cm from the head and the other 10 cm from the tail. These plate electrodes generated a field that was more or less homogenous around the body, and stimulated most elec-troreceptors that responded simultaneously. This electric field is termed the global field[13] and was used to search for electrosensory neurons.

After the electrosensory neurons responding to the global field were isolated, their responses to local electric fields generated by a dipole were measured. The dipole source was produced by two silver wires placed 5 mm apart under the rostrum of the animal. The wires were con-nected to a constant current source (A395 linear stimulus isolator; WPI, Sarasota, FL, USA) driven by a D/A con-verter (CED system, Micro 1401+; Cambridge, UK) with

a 10-kHz sampling frequency. Two dipoles of different orientations were applied to determine the neurons’ prefer-ence of field orientation. One dipolar orientation paralleled the rostro-caudal axis of the body (0°), and the other was perpendicular to the rostro-caudal axis (90°). The electrical fields were switched through the dipole by a switch array.

Sinusoidal wave stimuli at 0.1, 0.2, 0.5, 1, 2, 5 and 10 Hz with an amplitude of 25 µV/cm (frequency modulation), or at 5 Hz with amplitude varying continuously from 1 to 100 µV/cm (amplitude modulation) were delivered continuous-ly in the recording tank. The electric fields introduced into the tank were calibrated by measuring the voltage drop at 10 mm in the middle of the tank parallel to the field lines. The same setup was used in a previous study by Hofmann et al.[14]. Due to potential polarization effects, noise and direct-current offset, only large-amplitude fields were de-tectable. In this study, within the measurable range, there was a linear relation between the computer signal output (CED system) and the measured field magnitude. 2.3 Recording The activity of DON neurons was recorded with indium-alloy-filled glass electrodes (0.1–5 MΩ). As DON neurons may also respond to other stimuli, we col-lected data only from those electrosensory neurons that did not respond to visual (exposure to light from an electric torch), auditory (exposure to sound of clapping), or me-chanical stimuli. The signals were amplified 1 000 times, band-pass filtered at 100–10 kHz (DAM80; WPI, Sarasota, FL, USA), then displayed on an oscilloscope (DL1300A; Yokogawa, Tokyo, Japan) and monitored through the PC loudspeakers. A digital 50-Hz adaptive filter (Humbug; Quest Scientific, North Vancouver, Canada) was used to remove line noise. 2.4 Data analysis Data were analyzed using Spike 2 soft-ware (Wave Analysis; CED, Cambridge, UK). For sponta-neous activity, the discharge variability was quantified by the coefficient of variation (CV), the ratio of standard de-viation to mean interspike interval. A CV value of 1 means that the spike-train is random, and a lower value indicates a more regular spike-train.

For responses to sinusoidal wave fields with different frequencies and amplitudes, two parameters were calcu-

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lated. One was the relative discharge rate, i.e., the mean spike rate during the stimulation minus the spontaneous rate; this was calculated to determine the neurons’ sensitiv-ity. The other was the degree of phase-locking, which was obtained by computing the normalized period histogram of the phase angles of the spikes relative to the sine-wave cycle. Then, the value D was calculated, which is based on an estimate of the entropy of a period histogram and used as a measure of degree of phase-locking[15]. This value is 0 for random data and 1 if all spikes are in the same bin of the period histogram. For the period histogram of each neuron, all stimuli were repeated at least 5 times. The rela-tion between spontaneous rate and relative discharge rate or D value was plotted and analyzed.

3 Results

3.1 Spontaneous activity A total of 17 neurons from 12 white sturgeon were recorded, and the measured spontane-ous rates ranged from 0.41 to 98.54 Hz, with a mean rate of (14.94 ± 7.84) Hz. Twelve of the 17 neurons showed a mean rate above 10 Hz [(18.97 ± 4.83) Hz)], while 5 of the 17 had a mean rate lower than 10 Hz [(5.26 ± 3.98) Hz)]. Thus the neurons were classified into two types: those with a high spontaneous rate and those having a low spontaneous rate. The mean CV for all neurons was 0.4 ± 0.2, suggesting

Fig.1 Original recordings of DON neurons (A, B) during a 5-Hz sinusoidal stimulus (C). Each short line below the traces indicates a spike. The neuron with high spontaneous activity had a cluster of spikes in the positive cycle (A), while those with low spontaneous activity had only a single spike in the positive cycle (B).

that the spontaneous activity of the neurons was relatively regular. The mean CV values for the two types were 0.39 ± 0.25 (high spontaneous rate) and 0.56 ± 0.05 (low spontane-ous rate), and there was no significant difference between them (Mann-Whitney U test, U = 12.00, Z = -1.24, P >0.05).3.2 Response to sinusoidal wave stimulation The re-sponses of DON neurons to local dipole sinusoidal electric fields were measured, first with the dipole parallel to the rostro-caudal axis, placed under the ventral portion of the rostrum. Since most electroreceptors of the sturgeon lie in the ventral rostrum, the dipole field stimulated them all at the same time. The sine-wave field caused the DON neurons to modulate their firing rates with time. In most neurons, the firing was enhanced during the positive cycle of the sine-wave, and suppressed during the negative cycle (Fig. 1). In the neurons with low spontaneous activity, there were only one or two spikes in each positive cycle (Fig. 1B); and for those with high spontaneous activity, there was a cluster of firing in the positive cycle, but little firing in the negative cycle (Fig. 1A). This suggested that phase-locking occurred during the stimulus. It needs to be mentioned that in some neurons the firing was suppressed during the positive cycle of the sine-wave, and enhanced during the negative cycle.

In 12 DON neurons, the responses to a 5-Hz sinusoi-

Xuguang Zhang et al. Response properties of the electrosensory neurons in hindbrain of the white sturgeon, Acipenser transmontanus 425

dal dipole stimulus with 1–100 µV/cm peak-to-peak am-plitudes were tested. The evoked responses depended upon the magnitude of the stimuli. At high electric field mag-nitude, apparent phase-locked responses occurred, while at low amplitude, there was little evoked firing. Above 25 µV/cm, there was a significant increase in relative dis-charge rate (T-test, P = 0.009), with a maximum of 30 Hz (Fig. 2A). The D value, that denotes the degree of phase-locking, remained very low when the stimulus amplitude was low, but increased when the stimulus amplitude was >5 µV/cm (P = 0.008).

The DON neurons (n = 12) were also tested with sinusoidal fields at 0.1–10 Hz. In a previous study, the maximum stimulus amplitude was chosen as 25 µV/cm to compare the results from sturgeon with those from paddlefish[14]. However, here we found that this stimulus amplitude was too low to evoke reliable responses in stur-geon. The relative discharge rate barely changed (T-test, P >0.05), varying within a small range from -1 to 1 Hz (Fig. 3A). However, the degree of phase-locking (D value) showed a notable increase with frequency from 0.5 to 5 Hz (P = 0.03), with a slight decrease at 10 Hz (Fig. 3B).

Fig. 2 Responses of DON neurons (n = 12) to sinusoidal stimulation (5 Hz) at different amplitudes (1–100 μV/cm). A: When the amplitude was >25 μV/cm, the relative discharge rate showed a trend of increase at higher amplitudes (P <0.01). B: The D value also showed a trend of increase at higher am-plitudes, when the amplitude was >5 μV/cm (P <0.01).

Fig. 3 Responses of DON neurons (n = 12) to sinusoidal stimulation (25 μV/cm) at different frequencies (0.1–10 Hz). A: There was no significant change in relative discharge rate with sinusoidal field frequency at 0.1–10 Hz (P >0.05). B: The D value increased with higher frequencies within the range of 0.5–5 Hz (P <0.05).

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3.3 Responses to different dipole orientations The re-sponses to different dipolar orientations were also tested in all 12 DON neurons. For both dipole stimuli, all the neurons showed phase-locked responses as previously de-scribed, and increased their evoked discharge rates with a mean value of (8.07 ± 5.41) Hz at 0° and (6.74 ± 3.91) Hz at 90°; there was no significant difference between the rel-ative discharge rates at the two dipole orientations (Mann-Whitney U test, U = 6.00, Z = -0.577, P >0.05). However, four of 12 neurons showed an opposite phase-locking rela-tionship in the perpendicular dipole orientation. When the dipole paralleled the body axis, these neurons increased their spike rate at the positive half-cycle and had two peaks at angles of 200° and 270° in the phase plot (Fig. 4A). But when the dipole was perpendicular to the body axis, these neurons’ firing was suppressed at the positive cycle, and enhanced at the negative half-cycle at a phase angle of ap-proximately 90° (Fig. 4B).

4 Discussion

4.1 Electrosensory information-processing related to spontaneous activity In this study, the mean rate of spon-

Fig. 4 Phase plots of DON neurons. Average responses of the four neurons that showed an opposite phase-locking relationship in the perpendicular dipole orientation, to a dipole field with the orientation parallel (A) or perpendicular (B) to the rostro-caudal axis of the body, displayed as peristimulus time histograms. A: When the dipole paralleled the body axis, the neurons showed increased spike rates at the positive half-cycle and had two peaks at 200° and 270° in the phase plot. B: When the dipole was perpendicular to the body axis, these neurons’ firing was suppressed at the posi-tive half-cycle, and enhanced at the negative half-cycle at a phase angle of ~90°. Bin width: 5 ms. The insets indicate the orientation of the dipole field.

taneous activity in DON units of the white sturgeon was 15 Hz, which is substantially higher than the 1.2 Hz in elasmobranchs[12] and the 6 Hz in catfish[16]; but lower than that in paddlefish (31 Hz)[14]. Similar to paddlefish, the interspike intervals in the DON neurons of sturgeon had a mean CV lower than 1[14], suggesting relatively regular spontaneous firing.

In the present study, the responses of DON neurons to external electric field stimulation were characterized by relative discharge rate and D value (degree of phase-locking). The relative discharge rate increased with spon-taneous activity (Fig. 5A), but the degree of phase-locking decreased (Fig. 5B). This may have implications for neu-ronal information processing.

Although the spikes appeared as clusters during the positive or negative half-cycle of the electrical stimulus, the overall discharge rate changed only mildly. This sug-gests that the spontaneous rate acts as a carrier frequency in electrosensory information-processing. Carrier modula-tion also occurs in paddlefish, and the highest stimulus fre-quency must be lower than the mean rate to allow accurate coding in the signal bandwidth[17]. Thus, the neurons with

Xuguang Zhang et al. Response properties of the electrosensory neurons in hindbrain of the white sturgeon, Acipenser transmontanus 427

high spontaneous activity had the highest relative evoked rates during the stimulus. However, the degree of phase-locking decreased with the spontaneous rate. During the high-intensity stimulus experiments, some neurons showed saturation of their firing rates, even to the point of impair-ing information coding. Thus, the neurons with a low spontaneous rate would exhibit stronger phase-locking than those with a high spontaneous rate. It was suggested that the neurons with different spontaneous rates may act in different kinds of information-processing, i.e., via rate coding or phase coding.

Besides, when sinusoidal wave stimuli were applied in the mode of amplitude modulation, the neurons showed a trend of increased relative discharge rates at amplitudes above 25 µV/cm (Fig. 2A), and the D values also increased with amplitudes above 5 µV/cm (Fig. 2B). However, in response to frequency modulation at an amplitude of 25 µV/cm, the relative discharge rates changed little (Fig. 3A) while the degree of phase-locking increased with frequency (Fig. 3B). One reason may be that the intensity of the stimulus was too small to evoke a response in DON neurons[14]. Another is that DON neurons process information by phase-coding of a low-intensity stimulus. Hofmann et al. proposed that electrosen-sory information is processed as a first-derivative filter-based relative discharge rate in paddlefish. The derivative filter shifts

Fig. 5 A: The relationship of spontaneous rate to relative discharge rate. The relative discharge rate increased with spontaneous rate (n = 17). R2 = 0.126. B: The degree of phase-locking D value. The D value decreased with spontaneous rate (n = 17). R2 = 0.612.

the phase of the signal, but does not change the waveform[8]. However, our analysis was based on all the DON neurons, and could involve a combination of rate coding and phase coding.

If the two coding algorithms occur in different neurons, this would have important implications for electrosensory be-haviors. For example, electrosensory fish need a rapid response mechanism to avoid the high-intensity stimulus from predators or metal obstacles. Rate coding is more useful for a directional response and does not require complex computation. In prey-detection or mating, the rapid response of phase-locking may be helpful in electrosensory orientation. 4.2 Different responses in paddlefish and sturgeon Similar to the paddlefish, the sturgeon DON neurons showed amplitude and frequency tuning, but there were differences in response threshold. Unlike the small planktonic prey of paddlefish, the prey of sturgeon is much larger, including small fish and mollusks, and the maximal bioelectric field from these prey is up to 20 mV[18,19]. The response thresh-old of sturgeon was higher than that of paddlefish[13], which corresponds to their different prey. Some behavioral re-searchers claim that the sterlet A. ruthenus and the Russian sturgeon A. gueldenstaedtii orient and actively forage in electric fields ranging from 0.2 to 0.6 mV/cm[20]. For fre-quency tuning, both paddlefish and sturgeon show similar

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sensitive frequencies from 0.5 to 10 Hz. The frequencies of bioelectric fields from aquatic animals are usually in the range of 0.5 to a few Hertz[2]. The frequency tuning range of sturgeon DON neurons is also consistent with the fre-quency range of its prey.

In sturgeon, the DON neurons showed differential phase-locking at different dipolar directions (Fig. 4). The DON neurons always produced spikes that were phase-locked to the sine-wave, and the phase coupling varied among neurons. In catfish, two populations of cells with opposite response polarity were described in their lateral line lobes (equivalent to the DON)[16]. In paddlefish, neu-rons with opposite phase-locking relationships were found with the same stimulus, and may receive different informa-tion from fibers innervating the rostrum and gill cover[17]. 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. The bioelectric field was previ-ously elucidated as a type of dipole source with a positive head and a negative tail, or vice versa[21,22], suggesting that the selective response to differential dipolar direction is used in prey detection or conspecific interactions. Accurate phase coding is helpful in electrosensory orientation.

Acknowledgements: We thank Professors Horst Bleck-mann and Michael H. Hofmann in Bonn University for ex-perimental support. This work was supported by the National Natural Science Foundation of China (30970365), the Sci-ence and Technology Commission of Shanghai Municipality of China (073205109), Hydrobiology funding (S30701), and a grant from the Excellent Graduate Students Theses Culti-vation Program of Shanghai Municipality, China.

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高首鲟背听侧核电感受神经元在电场刺激下的反应特性

张旭光 1，Hendrik Herzog 2，宋佳坤 1，王晓杰 1，范纯新 1，郭弘艺 1

1上海海洋大学海洋生物系统与神经科学研究所，上海 2013062 波恩大学动物研究所，波恩 53115，德国

摘要：目的 软骨硬鳞鱼类的电感受是一种古老的感觉系统，它们通过电感受器官感受生物电场或非生物电场进

行摄食等活动。支配电感受器的初级传入神经首先将电感受信息传递至后脑的背听侧核进行处理。本文探讨了鲟

鱼背听侧核的电生理特性。方法 采用胞外记录方法记录了高首鲟背听侧核在偶极子电场刺激下的神经元反应。

结果 背听侧核神经元有低频(<10 Hz)自发放电和高频(>10 Hz)自发放电两种，在电场刺激下均产生明显的自发放

电的调制和相位耦合反应，同时部分神经元对偶极子电场的方向有选择性。结论 鲟鱼的电感受神经元反应特征

与其电感受的生物功能相适应。

关键词：电感受；鲟鱼；偶极子；神经元；后脑