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Sensitivity to novel feedback at different phases of a gymnotid electric organ discharge

Sensitivity to novel feedback at different phases of a gymnotid electric organ discharge

Fig. 1. Schematic diagram of the experimental arrangement (A) and examples of behavioral responses (B). (A) The experimental animal rested in a cage placed centrally, at half-water level, in a large tank. Two Ag/AgCl pellets, placed at the side of the fish at its trunk/tail region, could be connected, outside the tank, via a fast electronic switch. As a result of switch closure, a part of the electric organ discharge (EOD) current of the fish is redistributed to flow over the low-resistance path of the external circuit rather than through the water. This current could be monitored (cur) by inserting a current amplifier in the external circuit. As a reference of which electrocyte groups produced the current, head–tail EODs were recorded by two silver wires. To start an experiment, a rectangular pulse (en) simultaneously enabled a counter module (CT) and allowed EODs (sig) to be fed into a processor (PC). After 200 inter-EOD intervals were recorded, the counter module issued a reference pulse (ref), that signalled the onset of the 201st recorded EOD. By varying the delay of a command pulse (com) with respect to this reference pulse (DEL), the electronic switch could be closed during a selected phase of this particular EOD, or, as a control, in the silent time after it in which no EOD current is shunted. The processor continued to store 300 inter-EOD intervals that followed after switch closure. Prior to input to the counter module, the EODs were strongly amplified, filtered and converted to rectangular pulses (pulseformer; PF). The inset shows a head-to-tail EOD (sig; V 1 –V 4 denote the major phases
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Electric organ discharge diversity in the genus Gymnotus: anatomo functional groups and electrogenic mechanisms

Electric organ discharge diversity in the genus Gymnotus: anatomo functional groups and electrogenic mechanisms

The genus Gymnotus includes 37 species, distributed from Uruguay to as far north as southern Mexico (Crampton, 2011). These fishes, like other members of the order Gymnotiformes, exhibit the unusual ability to generate electric fields from a specialized electric organ (EO) controlled by the nervous system (Lissmann, 1958; Caputi et al., 2005; Caputi, 2011). The field generated by the electric organ discharge (EOD) is affected by the presence of nearby objects. Changes to the ongoing transcutaneous fields (electric images) are evaluated by an electrosensory array, allowing the fish to analyze the structure of nearby objects (Pereira and Caputi, 2010). In Gymnotus, the EOD field comprises a continuous train of pulses. Each pulse in the series is characterized by a stereotyped, species- specific waveform which serves as a communication signal (i.e. for mate attraction), in addition to its role as an electrolocation carrier (Black-Cleworth, 1970; Westby, 1974; McGregor and Westby, 1992; Crampton and Albert, 2006; Crampton et al., 2008; Crampton et al., 2011).
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Resolving competing theories for control of the jamming avoidance response: the role of amplitude modulations in electric organ discharge decelerations

Resolving competing theories for control of the jamming avoidance response: the role of amplitude modulations in electric organ discharge decelerations

The gymnotiform electric fish Eigenmannia emits quasi- sinusoidal discharges from its electric organ, located in the tail. These signals are used for electrolocation and electrocommunication (Heiligenberg, 1973; Hopkins, 1988). During electrolocation, fish maintain a constant, private frequency of electric organ discharge (EOD). They shift their otherwise constant frequencies of EOD when they encounter a neighbor whose EOD frequency is close to their own. The frequency shifts always occur in the direction that increases the frequency difference between a neighbor’s EOD and their own (Watanabe and Takeda, 1963; Bullock et al., 1972a,b). This ‘jamming avoidance response’ (JAR) serves to minimize the detrimental effects of foreign EODs on the animal’s electrolocation abilities (Heiligenberg, 1973). During jamming, fish are exposed to a complex signal mixture of the fish’s own and a neighbor’s EODs. Using information in this combined signal, fish are able to determine the correct direction to change their EOD frequency.
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Plasticity of the electric organ discharge: implications for the regulation of ionic currents

Plasticity of the electric organ discharge: implications for the regulation of ionic currents

Fig. 1. Schematic illustration of the electromotor circuit. (A) Extracellular field recordings from the pacemaker nucleus (PMN) and their relationship to the electric organ discharge (EOD) in Sternopygus. Each action potential in the PMN is followed by an EOD pulse. (B) The PMN is a midline medullary nucleus whose firing rate determines basal EOD frequency. The PMN drives spinal electromotor neurons (EMNs), which in turn drive the myogenically derived electrocytes in all families but the Apteronotidae, whose electric organ is composed of axons of the EMNs. Modulations of the basal EOD frequency are accomplished by glutamatergic inputs from the prepacemaker nucleus (PPn) and the sublemniscal prepacemaker nucleus (SPPn). (C) Pacemaker neurons, which are intrinsic to the nucleus, are electrotonically coupled to each other and drive relay neurons. The axons of the relay neurons run down the spinal cord and innervate the EMNs. The inputs from the PPn and SPPn activate pacemaker or relay cells via alpha-amino-3-hydroxy- 5-methyl-4 isoxazole proprionic acid (AMPA)- and N-methyl- D - aspartate (NMDA)-type glutamate receptors. There are species differences in these inputs and in the extent of electrotonic versus chemical coupling between pacemaker and relay cells. This figure shows the synaptology of the PMN of the genus Apteronotus. nE up ,
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Changes in electric organ discharge after pausing the electromotor system of Gymnotus carapo

Changes in electric organ discharge after pausing the electromotor system of Gymnotus carapo

The present study has demonstrated that the EOD of Gymnotus carapo undergoes a variety of changes when the electromotor system is reactivated after a pause. One of the most striking features of these post-pause changes is the time scale over which they occur: a rapid initial reduction in amplitude of 15 % may occur within less than 1 s. The subsequent slower rebuild to steady-state levels occurs within 1000 post-pause EODs or approximately 20 s. The changes are easy to study in unrestrained fish because G. carapo usually remains motionless during these periods and simple methods can be used for checking this. In the following discussion, an attempt is first made to interpret the post-pause changes in terms of a detailed model available for discharge generation in G. carapo (Caputi, 1999). The dynamics of the amplitude changes will then be described quantitatively by a simple heuristic model with activity-dependent kinetics.
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Effects of social interaction on the electric organ discharge in a
mormyrid fish, Gnathonemus petersii (Mormyridae, Teleostei)

Effects of social interaction on the electric organ discharge in a mormyrid fish, Gnathonemus petersii (Mormyridae, Teleostei)

African weakly discharging electric fish (family Mormyridae) use their self-generated electric signals [electric organ discharges (EODs)] and their electroreceptive abilities for orientation and communication (Hopkins, 1986; Moller, 1995; von der Emde, 1998; Rojas and Moller, 2002). EODs play a major role in territorial interactions (Kramer and Bauer, 1976; Crockett, 1986; Kramer, 1990). The waveform of the EOD does not vary appreciably over short time periods and thus potentially communicates the individual’s identity such as sex, species (Hopkins and Bass, 1981; Hopkins, 1983, 1986, 1988) and developmental state (Westby and Kirschbaum, 1977, 1978; Kirschbaum, 1987, 1995). Several species generate sexually dimorphic EODs, with mature males typically emitting longer EODs than females (e.g. Hopkins, 1980, 1981, 1986; Westby and Kirschbaum, 1982; Bass, 1986; Landsman, 1993a,b). Sexually immature males possess short, female-like EODs.
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The electric organ discharge of pulse gymnotiforms: the transformation of a simple impulse into a complex spatio temporal electromotor pattern

The electric organ discharge of pulse gymnotiforms: the transformation of a simple impulse into a complex spatio temporal electromotor pattern

An understanding of how the nervous system processes an impulse-like input to yield a stereotyped, species-specific electromotor output is relevant for electric fish physiology, but also for understanding the general mechanisms of coordination of effector patterns. In pulse gymnotids, the electromotor system is repetitively activated by impulse- like signals generated by a pacemaker nucleus in the medulla. This nucleus activates a set of relay cells whose axons descend along the spinal cord and project to electromotor neurones which, in turn, project to electrocytes. Relay neurones, electromotor neurones and electrocytes may be considered as layers of a network arranged with a lattice hierarchy. This network is able to coordinate a spatio-temporal pattern of postsynaptic and action currents generated by the electrocyte membranes. Electrocytes may be innervated at their rostral face, at
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The energetics of electric organ discharge generation in gymnotiform weakly electric fish

The energetics of electric organ discharge generation in gymnotiform weakly electric fish

Brain activity is thought to account for a significant fraction of the whole-animal resting metabolic rate: estimated at 5–7% in fish to 20% in humans (Mink et al., 1981). The high energetic cost is primarily due to the maintenance of membrane potentials, generation of action potentials and synaptic transmission (e.g. Attwell and Laughlin, 2001; Lennie, 2003; Niven and Laughlin, 2008; Harris et al., 2012). Weakly electric fish generate an electric signal to sense their environment and communicate with conspecifics over their entire lifetime. Because these signals are large relative to a typical neuronal action potential, it is reasonable to hypothesize that they would be metabolically costly. In fact, one previous study suggests that signalling in one species of electric fish is responsible for 60% of resting energy consumption (Nilsson, 1996). That said, other studies of these fish have not found a strong association between energy consumption and electric discharge properties (e.g. Julian et al., 2003). To better understand these apparent contradictions, as well as the role energetics may have played in the evolution of bioelectrogenesis and electrosensory processing in weakly electric fish, we present a bottom-up analysis of the associated energetic costs, followed by a comparative analysis of electric signal features.
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Electroreception in Gymnotus carapo: pre receptor processing and the distribution of electroreceptor types

Electroreception in Gymnotus carapo: pre receptor processing and the distribution of electroreceptor types

Fig. 7. Local fields associated with the self-generated electric organ discharge (LEOD) at the fovea (A,B) and on the trunk (C,D). LEODs were recorded with vertical and longitudinal orthogonal electrodes in the sagittal plane (A,C). The resulting field vectors were obtained by plotting the vertical field vectors as functions of the longitudinal vectors (B,D). Note that, at the fovea, the waveforms of the vertical and longitudinal components are similar (A), and current therefore flows along the same line throughout the OED (B). In contrast, on the trunk, the waveforms of the vertical and longitudinal components differ (C), and the current vectors therefore describe a loop (the sense of rotation is indicated by arrowheads) (D). The vector amplitude diminished from head to tail (E).
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Differences in electrosensory anatomy and social behavior in an area of sympatry between two species of mormyrid electric fishes

Differences in electrosensory anatomy and social behavior in an area of sympatry between two species of mormyrid electric fishes

Fig. 2. Electric organ discharge (EOD) waveforms were more variable among Gnathonemus victoriae than Petrocephalus degeni. (A) EOD waveforms of P. degeni and G. victoriae captured in Lwamunda Swamp. The EODs are amplitude-normalized and plotted head-positive up, with the EODs from different individuals superimposed and aligned to the head-positive peak. The same EODs are plotted on an expanded vertical scale below. (B) Frequency power spectra of the same EODs estimated using Welch ’ s averaged, modified periodogram method. Each trace is normalized to the maximum power. Bars above the traces show the average range of frequencies within 3 dB of the peak power frequency, along with the mean peak power frequency (±s.e.m.). (C) Box plots of maximum cross-correlation coefficients for all pair-wise EOD waveform comparisons. Within-individual comparisons were made by randomly selecting two EODs from the same individual; between-individual comparisons were made by randomly selecting an EOD from each of the two different individuals. Statistical comparisons were performed with Mann – Whitney U-tests. (D) Minimum polygons enclosing the EOD waveforms collected from G. victoriae and P. degeni plotted in bivariate signal space. An EOD was randomly selected from each individual of both species, followed by pair-wise cross-correlation between all these EODs. The maximum coefficients from all pair-wise cross-correlations were used to generate coordinates for each EOD using multidimensional scaling.
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Electrocyte physiology: 50 years later

Electrocyte physiology: 50 years later

Weakly electric gymnotiform and mormyrid fish generate and detect weak electric fields to image their worlds and communicate. These multi-purpose electric signals are generated by electrocytes, the specialized electric organ (EO) cells that produce the electric organ discharge (EOD). Just over 50  years ago the first experimental analyses of electrocyte physiology demonstrated that the EOD is produced and shaped by the timing and waveform of electrocyte action potentials (APs). Electrocytes of some species generate a single AP from a distinct region of excitable membrane, and this AP waveform determines EOD waveform. In other species, electrocytes possess two independent regions of excitable membrane that generate asynchronous APs with different waveforms, thereby increasing EOD complexity. Signal complexity is further enhanced in some gymnotiforms by the spatio-temporal activation of distinct EO regions with different electrocyte properties. For many mormyrids, additional EOD waveform components are produced by APs that propagate along stalks that connect postsynaptic regions to the main body of the electrocyte. I review here the history of research on electrocyte physiology in weakly electric fish, as well as recent discoveries of key phenomena not anticipated during early work in this field. Recent areas of investigation include the regulation of electrocyte activity by steroid and peptide hormones, the molecular evolution of electrocyte ion channels, and the evolutionary selection of ion channels expressed in excitable cells. These emerging research areas have generated renewed interest in electrocyte function and clear future directions for research addressing a broad range of new and important questions.
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Encoding phase spectrum for evaluating ‘electric qualia’

Encoding phase spectrum for evaluating ‘electric qualia’

Cues embodied in the changes of the phase spectra of the species-specific allo- and self-generated electric fields are relevant in pulse-emitting Mormyriformes for species and sex identification (Hopkins and Baas, 1981; Hopkins, 1986) and also to discriminate object impedance (von der Emde, f1990; von der Emde and Bleckmann, 1992; Gottwald et al., 2018). These teleosts possess an electrosensory path to sense the discharge of other fish (Bell and Grant, 1989). This path originates in the so-called knollenorgan receptors, which are mainly sensitive to the phase spectrum of the conspecific electric organ discharge (EOD) (Hopkins and Bass, 1981; Hopkins, 1986). There is another path originating in complex ‘ mormyromast receptors ’ innervated by two different types of fibers (Bell, 1990a, b) that show ‘ wide band ’ responsiveness to the amplitude spectrum (Bennett, 1967; Bell, 1990a, b). While one type of mormyromast-innervating fibers is only sensitive to stimulus strength, the other also responds to phase spectrum (von der Emde and Bleckmann, 1992). This dual (strength and phase) encoding has been related to impedance discrimination (von der Emde, 1990; von der Emde and Ronacher, 1994). Although two parameters are not enough to determine the impedance of an object, it has been shown that one can define families of impedance values that, independently of their position, modify reafferent signals in such a way that phase and strength are related by a linear function, defining an electric qualia likened to ‘ electric color ’ (Budelli and Caputi, 2000). Recent experimental evidence supports this hypothesis (Gottwald et al., 2018).
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Chirping and asymmetric jamming avoidance responses in the electric fish Distocyclus conirostris

Chirping and asymmetric jamming avoidance responses in the electric fish Distocyclus conirostris

Active sensory systems such as echolocation and electrolocation rely on accurate detection of small perturbations in self-generated signals and are sensitive to interference from signals produced by nearby conspecifics (Bullock et al., 1975; Ulanovsky et al., 2004; Nelson and MacIver, 2006). The jamming avoidance response (JAR) of South American weakly electric knifefish is a behavioral strategy thought to minimize deleterious interference caused by co-occurring signals (Watanabe and Takeda, 1963; Rose, 2004). Weakly electric fish generate weak electric fields by emitting an electric organ discharge (EOD) from a specialized electric organ. Fish can detect the position and properties of biotic and abiotic environmental features via localized distortions of the EOD (Lissmann, 1958; Heiligenberg, 1973; von der Emde, 1999). Additionally, social interactions with other electric fish create complex distortions of the field (Scheich, 1977; Zakon et al., 2002). When two fish are in close proximity, each fish perceives the other ’ s EOD by the interference created when the other fish ’ s EOD interacts with its own. The regular constructive and destructive interference
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Beyond the Jamming Avoidance Response: weakly electric fish respond to the envelope of social electrosensory signals

Beyond the Jamming Avoidance Response: weakly electric fish respond to the envelope of social electrosensory signals

Recent studies have shown that central nervous system neurons in weakly electric fish respond to artificially constructed electrosensory envelopes, but the behavioral relevance of such stimuli is unclear. Here we investigate the possibility that social context creates envelopes that drive behavior. When Eigenmannia virescens are in groups of three or more, the interactions between their pseudo-sinusoidal electric fields can generate ʻsocial envelopesʼ. We developed a simple mathematical prediction for how fish might respond to such social envelopes. To test this prediction, we measured the responses of E. virescens to stimuli consisting of two sinusoids, each outside the range of the Jamming Avoidance Response (JAR), that when added to the fishʼs own electric field produced low-frequency (below 10  Hz) social envelopes. Fish changed their electric organ discharge (EOD) frequency in response to these envelopes, which we have termed the Social Envelope Response (SER). In 99% of trials, the direction of the SER was consistent with the mathematical prediction. The SER was strongest in response to the lowest initial envelope frequency tested (2  Hz) and depended on stimulus amplitude. The SER generally resulted in an increase of the envelope frequency during the course of a trial, suggesting that this behavior may be a mechanism for avoiding low-frequency social envelopes. Importantly, the direction of the SER was not predicted by the superposition of two JAR responses: the SER was insensitive to the amplitude ratio between the sinusoids used to generate the envelope, but was instead predicted by the sign of the difference of difference frequencies.
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Electrocommunication signals in free swimming brown ghost knifefish,
Apteronotus leptorhynchus

Electrocommunication signals in free swimming brown ghost knifefish, Apteronotus leptorhynchus

Brown ghost knifefish, Apteronotus leptorhynchus , are a species of weakly electric fish that produce a continuous electric organ discharge (EOD) that is used in navigation, prey capture and communication. Stereotyped modulations of EOD frequency and amplitude are common in social situations and are thought to serve as communication signals. Of these modulations, the most commonly studied is the chirp. This study presents a quantitative analysis of chirp production in pairs of free-swimming, physically interacting male and female A. leptorhynchus . Under these conditions, we found that in addition to chirps, the fish commonly produce a second signal type, a type of frequency rise called abrupt frequency rises, AFRs. By quantifying the behaviours associated with signal production, we find that Type 2 chirps tend to be produced when the fish are apart, following periods of low aggression, whereas AFRs tend to be produced when the fish are aggressively attacking one another in close proximity. This study is the first to our knowledge that quantitatively describes both electrocommunication signalling and behavioural correlates on a subsecond time-scale in a wave-type weakly electric fish.
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Waveform discrimination, phase sensitivity and jamming avoidance in a wave type electric fish

Waveform discrimination, phase sensitivity and jamming avoidance in a wave type electric fish

The electric organ discharge (EOD) of most species of the freshwater knifefishes (Gymnotiformes) of South America is of the wave, not the pulse, type. Wave EODs are usually of constant frequency and amplitude, and show a bewildering multitude of species-characteristic waveforms. The EOD of Eigenmannia is sexually dimorphic in waveform and in the intensity of its higher harmonics. In a go/no go paradigm, trained food-rewarded fish discriminated between these waveforms, and naive (untrained) fish showed a significant preference. To determine whether spectral or waveform (time) cues are used by the fish, artificial stimuli of identical amplitude spectrum were synthesized that differed only in phase relationship between their harmonics, i.e. waveform, and the fish discriminated even among these stimulus waveforms (i.e. spectral cues are not required). Our sensory model predicts that, for successful waveform detection, a minimum frequency difference is required between the stimulus and the EOD. As expected, trained fish confused test stimuli of different waveform that were
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Development and regeneration of the electric organ

Development and regeneration of the electric organ

Electric organs and the neuronal control pathways that activate them have evolved multiple times in the evolution of fishes. This represents a paradigm case for how established organs and cell types become transformed by specific developmental processes to acquire new functions over evolutionary time and how this may occur independently in multiple lineages. Using the regeneration of the electric organ after amputation of the tail, we have shown that the large electrocytes of the weakly electric teleost Sternopygus derive from the fusion of numerous smaller muscle fibers. The newly formed electrocytes then down-regulate many muscle-specific proteins and organelles and become specialized for fine control of electrical excitability. Silencing or removing the neural input to the electrocytes causes them to re-express the muscle phenotype. A major quest for the future is understanding the co-evolution of the processes by which motor neurons produce, and muscle fibers respond to, specific signals for this phenotype transformation.
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Electric organ discharges and electric images during electrolocation

Electric organ discharges and electric images during electrolocation

resulting from the fish’s discharge and environment. Because electrosensory input patterns are highly dependent on the EOD pattern, we have re-examined in detail the autogenous EODs. In the first section below, we present and interpret EOD maps for several gymnotiform species. In the second section, we describe computer simulations designed to reconstruct electric images resulting from external objects and the fish’s exploratory behaviors. Electric images depend on many variables, including the fish’s EOD, the electrical impedance of its body and skin, water resistivity, the impedance and geometry of the object and the location, configuration and velocity of the body and object. We have used semi-analytical simulations of static electric images to propose algorithms for extracting sets of object features (e.g. their size, distance, impedance, shape) from sets of electric image features (e.g. position, amplitude, spread, phase). To examine natural dynamic behaviors and to predict sequences of electric images from electric fish exploring novel objects, we have developed a more general three-dimensional electric field simulator. Our results suggest how the fish’s probing movements could help it recognize object features. Our detailed field maps and electric field simulators are powerful new tools for exploring the neurocomputational algorithms for electrolocation. In the final section below, we discuss an electrolocation model based on feature sets and algorithms revealed by systematic analyses of electric images. The preliminary model and its predictions may help guide electrophysiological experiments exploring the neural basis of electrolocation.
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Waveform generation in the weakly electric fish Gymnotus
coropinae (Hoedeman): the electric organ and the electric organ
discharge

Waveform generation in the weakly electric fish Gymnotus coropinae (Hoedeman): the electric organ and the electric organ discharge

We used two recording procedures: (1) the longitudinal head to tail EOD (htEOD) fields, recorded using two silver/silver chloride electrodes, each placed on the middle line of the tank at different distances (steps of 4 cm up to the limits of the tank), one in front of the head and the other behind the tail; (2) the near-field recordings (Local EOD, LEOD) were measured using a specially designed LEOD probe placed close to the skin of the fish at different points along its body. The latter technique (for details, see Aguilera et al., 2001; Rodríguez-Cattáneo et al., 2008) was used to record local potential gradients equivalent to the orthogonal components of the local electric field vector at that point. The LEOD probe was constructed from three wires, insulated except at their tips. Active electrodes were oriented along horizontal orthogonal axes (perpendicular and parallel to the main body axis) intersected at the point where the reference was placed (facing the point on the skin under investigation). The tip of the active electrodes was 2.5 mm from the reference electrode. We carried out two types of experiments. First we recorded LEODs of the head region at equally spaced points (2 mm steps) along a parasagittal line passing 2 mm from the nearest point on the fish skin surface at the middle of the fish height. Second, we recorded the field at equally spaced points (1 cm steps) along five parasagittal lines separated, respectively, 1, 2, 3, 4 or 5 cm from the fish’s nearest point. ‘Vector plots’ were constructed for every sampled time of the EOD using the two simultaneous orthogonal fields obtained at each and every recording position.
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Experimental Study of Electric and Spectroscopic Characteristics of Electric Discharge in LPG

Experimental Study of Electric and Spectroscopic Characteristics of Electric Discharge in LPG

The electric and spectroscopic characteristics of electric discharge have been used to explore the discharge me- chanisms in LPG. A deviation from Paschen’s law has been reported which has been attributed to the diffusion outside the discharge volume of the active species of secondary processes such as photons and excited atoms. The discharge has a repetitive behaviour where each cycle consists of three phases; discharge off, glow discharge and spark discharge. The repetition frequency of the discharge covers a wide range from 5 kHz to 5 MHz which de- pends on the applied voltage and the gas pressure. It is concluded that the present discharge modes are very useful for the dissociation of LPG molecules. Hydrogen atoms, C 2 molecule and CH radical have been detected in the
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