Interdischarge Interval Research Articles

Distinct patterns of interictal intracranial EEG in focal cortical dysplasia type I and II

ObjectiveFocal cortical dysplasia (FCD) is the most common malformation causing refractory focal epilepsy. Surgical removal of the entire dysplastic cortex is crucial for achieving a seizure-free outcome. Precise presurgical distinctions between FCD types by neuroimaging are difficult, mainly in patients with normal magnetic resonance imaging findings. However, the FCD type is important for planning the extent of surgical approach and counselling. MethodsThis study included patients with focal drug-resistant epilepsy and definite histopathological FCD type I or II diagnoses who underwent intracranial electroencephalography (iEEG). We detected interictal epileptiform discharges (IEDs) and their recruitment into repetitive discharges (RDs) to compare electrophysiological patterns characterizing FCD types. ResultsPatients with FCD type II had a significantly higher IED rate (p < 0.005), a shorter inter-discharge interval within RD episodes (p < 0.003), sleep influence on decreased RD periodicity (p < 0.036), and longer RD episode duration (p < 0.003) than patients with type I. A Bayesian classifier stratified FCD types with 82% accuracy. ConclusionTemporal characteristics of IEDs and RDs reflect the histological findings of FCD subtypes and can differentiate FCD types I and II. SignificancePresurgical prediction of FCD type can help to plan a more tailored surgical approach in patients with normal magnetic resonance findings.

A method for editing motor unit potential trains obtained by decomposition of surface electromyographic signals

Rather than discarding motor unit potential trains (MUPTs) because they do not meet 100% validity criteria, we describe and evaluate a novel editing routine that preserves valid discharge times, based on decreasing shape variability (variance ratio, VR) within a MUPT. The error filtered estimation (EFE) algorithm is then applied to the remaining ‘high confidence’ discharge times to estimate inter-discharge interval (IDI) statistics. Decomposed surface EMG data from the flexor carpi radialis recorded from 20 participants during 60% MVC wrist flexion was used. There were two levels of denoising criteria (relaxed and strict) criteria for removing MUPs to decrease the VR and increase the signal-to-noise ratio (SNR) of a MUPT. In total, VR decreased 24.88% and SNR increased 6.0% (p’s < 0.05). The MUP template peak-to-peak (P-P) amplitude and P-P duration were dependent on the level of denoising (p’s < 0.05). The standard error of the estimate (SEE) of the mean IDI before and after editing using the relaxed criteria (3.2% versus 3.69%), was very similar (p > 0.05). The same was true for the SEE between denoising criteria, which increased only to 5.14% for the strict criteria (p > 0.05). Editing the MUPTs resulted in a significant decrease in MUP shape variability and in the measures extracted from the MUP templates, with trivial differences between the SEE of the mean IDI between the edited and unedited MUPTs.

Exact inter-discharge interval distribution of motor unit firing patterns with gamma model

Inter-discharge interval distribution modeling of the motor unit firing pattern plays an important role in electromyographic decomposition and the statistical analysis of firing patterns. When modeling firing patterns obtained from automatic procedures, false positives and false negatives can be taken into account to enhance performance in estimating firing pattern statistics. Available models of this type, however, are only approximate and use Gaussian distributions, which are not strictly suitable for modeling renewal point processes. In this paper, the theory of point processes is used to derive an exact solution to the distribution when a gamma distribution is used to model the physiological firing pattern. Besides being exact, the solution provides a way to model the skewness of the inter-discharge distribution, and this may make it possible to obtain a better fit with available experimental data. In order to demonstrate potential applications of the model, we use it to obtain a maximum likelihood estimator of firing pattern statistics. Our tests found this estimator to be reliable over a wide range of firing conditions, whether dealing with real or simulated firing patterns, the proposed solution had better agreement than other models.Graphical Model of the MU firing pattern generation and detection: fT,1(τ), IDI PDF of the physiological firing pattern; fT(τ), IDI PDF after modeling undetected firings (false negatives); fS(τ), IDI PDF after modeling classification errors (false positives)

GABAA Receptor Activity Suppresses the Transition from Inter-ictal to Ictal Epileptiform Discharges in Juvenile Mouse Hippocampus

Exploring the transition from inter-ictal to ictal epileptiform discharges (IDs) and how GABAA receptor-mediated action affects the onset of IDs will enrich our understanding of epileptogenesis and epilepsy treatment. We used Mg2+-free artificial cerebrospinal fluid (ACSF) to induce epileptiform discharges in juvenile mouse hippocampal slices and used a micro-electrode array to record the discharges. After the slices were exposed to Mg2+-free ACSF for 10min-20min, synchronous recurrent seizure-like events were recorded across the slices, and each event evolved from inter-ictal epileptiform discharges (IIDs) to pre-ictal epileptiform discharges (PIDs), and then to IDs. During the transition from IIDs to PIDs, the duration of discharges increased and the inter-discharge interval decreased. After adding 3μmol/L of the GABAA receptor agonist muscimol, PIDs and IDs disappeared, and IIDs remained. Further, the application of 10μmol/L muscimol abolished all the epileptiform discharges. When the GABAA receptor antagonist bicuculline was applied at 10μmol/L, IIDs and PIDs disappeared, and IDs remained at decreased intervals. These results indicated that there are dynamic changes in the hippocampal network preceding the onset of IDs, and GABAA receptor activity suppresses the transition from IIDs to IDs in juvenile mouse hippocampus.

Generalized Periodic Discharges: A Topical Review.

Generalized periodic discharges (GPDs) are generalized discharges that recur with a relatively uniform morphology and duration. They have a quantifiable interdischarge interval. Over the past decade, our understanding of these waveforms has improved considerably. The nomenclature has changed, and etiologic references have been removed. Many disease states can cause GPDs, such as anoxia, toxic/metabolic encephalopathy, infections, nonconvulsive status epilepticus, and hypothermia. Generally, GPDs are morphologically similar regardless of etiology. Generalized periodic discharges that are associated with nonconvulsive status epilepticus are treated with antiseizure drugs, while others are not necessarily aggressively treated. Prognosis for most patients with GPDs is guarded, although this is also dependent on the underlying etiology. As our understanding of GPDs increases, it is also clear that there is much more to be learned about these waveforms.

Characteristics of Epileptiform Discharge Duration and Interdischarge Interval in Genetic Generalized Epilepsies.

We sought to investigate (1) the characteristics of epileptiform discharge (ED) duration and interdischarge interval (IDI) and (2) the influence of vigilance state on the ED duration and IDI in genetic generalized epilepsy (GGE). In a cohort of patients diagnosed with GGE, 24-h ambulatory EEG recordings were performed prospectively. We then tabulated durations, IDI, and vigilance state in relation to all EDs captured on EEGs. We used K-means cluster analysis and finite mixture modeling to quantify and characterize the groups of ED duration and IDI. To investigate the influence of sleep, we calculated the mean, median, and SEM in each population from all subjects for sleep state and wakefulness separately, followed by the Kruskal–Wallis test to compare the groups. We analyzed 4,679 EDs and corresponding IDI from 23 abnormal 24-h ambulatory EEGs. Our analysis defined two populations of ED durations and IDI: short and long. In all populations, both ED durations and IDI were significantly longer in wakefulness. Our results highlight different characteristics of ED populations in GGE and the influence by the sleep–wake cycle.

Electrographic Features of Lateralized Periodic Discharges Stratify Risk in the Interictal-Ictal Continuum.

To risk-stratify electrographic features of lateralized periodic discharges (LPDs) in acute structural brain lesions for predictors of electrographic seizures. This is a retrospective review of 100 consecutive patients with LPDs. Epileptiform features of LPDs were described based on electrographic features: blunt delta morphology, sharply contoured, overlying fast frequencies, and/or rhythmicity (loss of interdischarge interval lasting ≥1 second). EEG seizures were defined as evolving in frequency, distribution, or morphology at ≥2 Hz for ≥10 seconds. Overall, electrographic seizures occurred in 55% of patients with LPDs. Lateralized periodic discharges with rhythmicity (odds ratio 13.91) were most significant for predicting status epilepticus and/or seizures. This was followed by LPDs with overlying faster frequencies (odds ratio 5.16) and then sharply contoured morphology (odds ratio 4.09). Blunt delta morphology (0.24) had the lowest risk for seizures. Electrographic features of LPDs may help determine seizure risk in patients with acute structural lesions. Sharply contoured morphology, overlying fast frequencies, or rhythmicity, showed progressively higher risk of seizures on continuous electroencephalography, whereas blunt delta morphology had the lowest risk of seizures.

58. Electroencephalographic findings in a patient with catatonia, secondary to delayed encephalopathy due to carbon monoxide exposition

Objective To demonstrate electroencephalographic evolution in catatonia, secondary to carbon monoxide poisoning. Case report A 28-year-old female, with accidental carbon monoxide exposition, showed drowsiness and motor focal seizures in right limbs, acutely. After 3 weeks, she presented with headache, memory dysfunction, and catatonic syndrome. Brain MRI showed bilateral frontoparietal hyper intensities in T2 and FLAIR with left predominance and associated restricted diffusion. Electroencephalographic evolution: The first EEG (after seizures) showed PLEDs, characterized by biphasic waves in left frontocentral region with an inter-discharge interval of 0.5–1 s. Second EEG (a week later, receiving treatment with amantadine and lorazepam), showed diffuse slowing without PLEDs. Third EEG, one month after the exposure, and complete clinical recovery, was normal. Comment The EEG in a patient with monoxide carbon and catatonia can show nonspecific findings, showing the most significant changes in the acute phase of the intoxication, and it proves to be useful in the differential diagnosis of catatonia.

Inter-discharge interval distribution of motor unit firing patterns with detection errors.

Inter-discharge interval (IDI) distribution analysis of motor unit firing patterns is a valuable tool in EMG decomposition and analysis. However, the firing pattern obtained by EMG decomposition may have detection errors: false positives (incorrectly classified firings) and false negatives (missed firings). In this paper, the mathematical derivation of an IDI distribution model that accommodates false positives and false negatives of the detection process is presented. An approximation of the general model to adapt to specific EMG decomposition conditions is also presented. To illustrate the usefulness of the model, the obtained distribution is used to derive the maximum likelihood estimates of the statistics of motor unit firing patterns, the IDI mean and standard deviation, and estimates of the false negative and false positive ratios. Results obtained from simulation experiments and tests with real motor unit firing patterns show an enhanced estimation performance when compared to previously available algorithms. Goodness-of-fit tests applied to estimations for real data corrupted with false positives showed that the model-driven estimations fitted the uncorrupted data better than EFE estimations: 82% versus 52% not rejectable, respectively, when false positives were about 10% of IDIs. With about 5% false positives, the not rejectable estimations were 85% versus 70%.

Myotonic discharges discriminate chloride from sodium muscle channelopathies

Non-dystrophic myotonic syndromes represent a heterogeneous group of clinically quite similar diseases sharing the feature of myotonia. These syndromes can be separated into chloride and sodium channelopathies, with gene-defects in chloride or sodium channel proteins of the sarcolemmal membrane. Myotonia has its basis in an electrical instability of the sarcolemmal membrane. In the present study we examine the discriminative power of the resulting myotonic discharges for these disorders.Needle electromyography was performed by an electromyographer blinded for genetic diagnosis in 66 non-dystrophic myotonia patients (32 chloride and 34 sodium channelopathy). Five muscles in each patient were examined. Individual trains of myotonic discharges were extracted and analyzed with respect to firing characteristics.Myotonic discharge characteristics in the rectus femoris muscle almost perfectly discriminated chloride from sodium channelopathy patients. The first interdischarge interval as a single variable was longer than 30 ms in all but one of the chloride channelopathy patients and shorter than 30 ms in all of the sodium channelopathy patients. This resulted in a detection rate of over 95%.Myotonic discharges of a single muscle can be used to better guide toward a molecular diagnosis in non-dystrophic myotonic syndromes.

Maximum likelihood estimation of motor unit firing pattern statistics.

Estimation of motor unit firing pattern statistics is a valuable method in physiological studies and a key procedure in electromyographic (EMG) decomposition algorithms. However, if any firings within the pattern are undetected or missed during the decomposition process, the estimation procedure can be disrupted. In order to provide an optimal solution, we present a maximum likelihood estimator of EMG firing pattern statistics, taking into account that some firings may be undetected. A model of the inter-discharge interval (IDI) probability density function with missing firings has been employed to derive the maximum likelihood estimator of the mean and standard deviation of the IDIs. Actual calculation of the maximum likelihood solution has been obtained by means of numerical optimization. The proposed estimator has been evaluated and compared to other previously developed algorithms by means of simulation experiments and has been tested on real signals. The new estimator was found to be robust and reliable in diverse conditions: IDI distributions with a high coefficient of variance or considerable skewness. Moreover, the proposed estimator outperforms previous algorithms both in simulated and real conditions.

Electrocommunication behaviour during social interactions in two species of pulse‐type weakly electric fishes (Mormyridae)

This study compares electrocommunication behaviour in groups of freely swimming weakly electric fishes of two species, Marcusenius altisambesi and Mormyrus rume. Animals emitted variable temporal sequences of stereotyped electric organ discharges (EOD) that served as communication signals. While the waveform of individual signals remained constant, the inter-discharge interval (IDI) patterns conveyed situation-specific information. Both species showed different types of group behaviour, e.g. they engaged in collective (group) foraging. The results show that in each species, during different behavioural conditions (resting, foraging and agonistic encounters), certain situation-specific IDI patterns occurred. In both species, neighbouring fishes swimming closely together interacted electrically by going in and out of synchronization episodes, i.e. periods of temporally correlated EOD production. These often resulted in echo responses between neighbours. During group foraging, fishes often signalled in a repetitive fixed order (fixed-order signalling). During foraging, EOD emission rates of M. altisambesi were higher and more regular than those of M. rume. The two species also differed in the quantity of group behaviours with M. altisambesi being more social than M. rume, which was reflected in the lack of specific agonistic IDI patterns, more fixed-order signalling and more communal resting behaviour in M. altisambesi.

Period doubling bifurcation in a train of spontaneous activity

Introduction: It has been shown that fibrillations (FIBs) and positive sharp waves (PSWs) occur during spontaneous oscillations of the membrane potential when the threshold is reached. According to the models of excitable membranes these oscillations should be nonlinear. We wondered whether the nonlinearity of the underlying process could also be demonstrated indirectly in the pattern of spontaneous discharges that can be recorded much easier extracellularly in routine electromyography. A simple example of nonlinear behaviour is a period doubling bifurcation in a periodic system. Methods: In our clinical neurophysiology laboratory discharges are saved on hard disc and the interval between successive discharges is analyzed if there is any doubt whether the discharges occur at regular intervals. In one recording out of 32 we found a phenomenon that we believe to represent a bifurcation. The recording is from the left anterior tibial muscle of a 67 year old patient. The patient showed widespread presence of spontaneous activity and fasciculations in muscles. Neurography was normal. Thus, a motor neuron disease was suspected. The recordings were made with the commercial Neurophysiology workstation „Keypoint“ from ALPINE Biomed with concentric needle electrodes. The samples were exported in ASCII format at a sampling frequency of 24kHz and a resolution of 1µV. Discharges were selected manually and the interdischarge interval (IDI) was calculated. Results: The upper trace in Fig.1 shows the signal as recorded with the concentric needle electrode. The peaks of the discharges that were used to calculate the interdischarge intervals are marked with little circles. The lower trace shows the interdischarge intervals as a function of time. Note that the discharge intervals decrease initially, and increase slowly afterward. At the moment indicated by the double arrow two different IDIs occur that alternate. This resembles behaviour resembles very closely period doubling bifurcations that can be observed in simple nonlinear systems such as the logistic map. Discussion: The recording presented here illustrates that irregularity at the end of trains of spontaneous activity can be the result of nonlinear deterministic behaviour. Further studies have to show whether more irregular behaviour that also can be observed at the end of these trains can also be described with methods of nonlinear dynamics.

A male’s playback signal turns female Marcusenius pongolensis receivers on or off depending on his behavioral state

The electric organ discharges (EODs) of male southern bulldog fish, Marcusenius pongolensis, are of longer pulse duration than those of females, and grow with body size.1 In a playback experiment, male EODs of longer pulse duration were more attractive to females in terms of association time and other behavioral variables.2 Here, we show that the greater attraction of long male EODs to females was only revealed when combined with ‘acceptable’ information on his behavioral state (the combination was manipulated experimentally). Females were attracted to long EODs had the male (apparently) been in a nocturnally-active but non-aggressive behavioral state, but the preference vanished when in a diurnally ‘resting’ or nocturnal aggression (agonistic) state. Information on male behavioral state was conveyed to females by one of four types of inter-discharge interval (IDI) pattern that were used to drive the presentation of EODs.

Electric communication during courtship and spawning in two sibling species of dwarf stonebasher from southern Africa, Pollimyrus castelnaui and P. marianne (Mormyridae, Teleostei): evidence for a non species-specific communication code?

The fixed part of the electrocommunication signal, the electric organ discharge (EOD) waveform, is well differentiated in the two vicariant dwarf stonebasher species, Pollimyrus castelnaui and P. marianne. However, differentiation regarding the variable, situation-dependent part, i.e., inter-discharge interval (IDI) patterns, has never been studied in a pair of sibling species of mormyrid fish. We here compare the electrical signalling that accompanies different motor behaviours (such as resting and swimming, territorial agonistic interactions, courtship and spawning) in the two species. Double pulse patterns of regularly alternating short IDIs of 8-11 ms and long ones of 16-100 ms accompanied threat displays in both species. In three pairs of P. marianne and five pairs of P. castelnaui, courtship was characterised by nest building, territory patrolling and acoustic displays (advertisment calls) that were accompanied by long discharge breaks in the male and highly regular IDIs around 50 ms in the female of both species. Nest-tending males showed IDI sequences consisting of regularly alternating double pulse patterns, similar to threat displays. During spawning both sexes generated stereotyped IDI sequences of a low discharge rate. All IDI patterns occurring in one species were also found in the other, and no species-specifity was identified at that level. Playback experiments contrasting conspecific and heterospecific IDI sequences (that had been recorded from nocturnally swimming fish) revealed preferences in none of the six experimental subjects. Double pulse patterns, high discharge rate displays (HD) and regularisations of the IDI sequence accompanying specific behaviours occurred in similar form in both dwarf stonebasher species of the present study. Therefore, we conclude that in the speciation of P. castelnaui and P. marianne the fixed part of the EOD, its waveform, was under more differential selection pressure than its variable part, the patterns of IDI.

Interspike interval correlations, memory, adaptation, and refractoriness in a leaky integrate-and-fire model with threshold fatigue.

Neuronal adaptation as well as interdischarge interval correlations have been shown to be functionally important properties of physiological neurons. We explore the dynamics of a modified leaky integrate-and-fire (LIF) neuron, referred to as the LIF with threshold fatigue, and show that it reproduces these properties. In this model, the postdischarge threshold reset depends on the preceding sequence of discharge times. We show that in response to various classes of stimuli, namely, constant currents, step currents, white gaussian noise, and sinusoidal currents, the model exhibits new behavior compared with the standard LIF neuron. More precisely, (1) step currents lead to adaptation, that is, a progressive decrease of the discharge rate following the stimulus onset, while in the standard LIF, no such patterns are possible; (2) a saturation in the firing rate occurs in certain regimes, a behavior not seen in the LIF neuron; (3) interspike intervals of the noise-driven modified LIF under constant current are correlated in a way reminiscent of experimental observations, while those of the standard LIF are independent of one another; (4) the magnitude of the correlation coefficients decreases as a function of noise intensity; and (5) the dynamics of the sinusoidally forced modified LIF are described by iterates of an annulus map, an extension to the circle map dynamics displayed by the LIF model. Under certain conditions, this map can give rise to sensitivity to initial conditions and thus chaotic behavior.

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

During their entire lives, weakly electric fish produce an uninterrupted train of discharges to electrolocate objects and to communicate. In an attempt to learn about activity-dependent processes that might be involved in this ability, the continuous train of discharges of intact Gymnotus carapo was experimentally interrupted to investigate how this pausing affects post-pause electric organ discharges. In particular, an analysis was conducted of how the amplitude and relative timing of the three major deflections of the complex discharge change over the course of the first 1000 post-pause discharges. The dependence of these variables on the duration of the preceding pause and on water temperature is analysed. In addition, pause-induced small reverberations at the end of the discharge are described. Common to all amplitude changes is a fast initial decrease in amplitude with a slow recovery phase; amplitude changes scale with the duration of the preceding pause and are independent of the interdischarge interval. The absence of changes in the postsynaptic-potential-derived first phase of the discharge together with changes in the amplitude ratio of the third and fourth deflections suggest that the amplitude changes are mainly due to pause-induced changes in the inner resistance of the electric organ. A model is formulated that approximates the pattern of amplitude changes. The post-pause changes described here may provide a new way to test current models of complex discharge generation in Gymnotus carapo and illustrate the speed at which changes of an electric organ discharge can take place.

Cortical excitability and recovery curve analysis in generalized epilepsy.

Seven untreated patients with idiopathic generalized epilepsy were studied with recovery curve analysis using transcranial magnetic stimulation and compared with 16 controls. Patients had a shorter period of inhibition of the test response following a conditioning stimulus and demonstrated a period of increased facilitation of the test response at interstimulus intervals of 200 to 300 msec, which was similar to the mean interdischarge interval of spike-wave activity on EEG. This provides further evidence of cortical hyperexcitability in idiopathic generalized epilepsy.

Species recognition by the sequence of discharge intervals in weakly electric fishes of the genus Campylomormyrus (Mormyridae, Teleostei)

Abstract. In two Campylomormyrus species, tamandua and rhynchophorus from Central Africa, the electric organ discharge (EOD) activity was studied during the nocturnal activity phase in the laboratory. Both species have a pulse-type EOD of less than 200 μs duration and similar waveform; the sequence of inter-discharge intervals, however, differed characteristically: C. tamandua displayed a 'micro-pattern' encompassing nearly the whole range of intervals in a sequence of only three intervals (long-intermediate-short), while in C. rhynchophorus adjacent intervals tended to be more similar in duration. Four C. rhynchophorus and five C. tamandua were tested for their preference of conspecific pulse sequences rather than those of the other species, respectively, in playback experiments. These were performed in a T-maze paradigm such that two pulse patterns, one from each species, were simultaneously presented via two electric fish dipole models. Two pulse sequences recorded from different individuals were used to represent each species; the natural EOD waveform was replaced by a square-wave pulse of approximately natural duration. The pattern pairings and the sequence of stimulus patterns followed a randomized blocks design. Each of the four C. rhynchophorus had significantly higher preference scores for the conspecific pulse patterns than for those of C. tamandua, while in C. tamandua no such discrimination was observed. It is suggested that the juvenile C. tamandua used would probably have joined mixed-species schools as reported to exist in the wild, while this appears unlikely in the more mature C. rhynchophorus. One of the functions of the inter-discharge interval code of communication in mormyrids is species recognition although this may be seen only in sufficiently mature fish.

Jitter measurement by axonal micro-stimulation. Guidelines and technical notes

Single fiber EMG (SFEMG) with axonal micro-stimulation is a convenient method to study the neuromuscular jitter at the individual motor end-plates. Compared to the original method of jitter measurement in voluntarily activated muscle, it has the advantage of perfect control of the discharge rate, including pauses in activity, useful in quantitative estimation of the neuromuscular transmission defect. It obviates the need to search for muscle fiber pairs. It can be used in young children and in uncooperative patients, as well as those with impaired voluntary motor control. It is useful in animal experiments as well as veterinary medicine. The technique eliminates the possibility of overestimating the jitter due to unrecognized interdischarge interval dependent jitter, as well as that of underestimating it due to unrecognized low jitter in split muscle fibers. The technique has certain pitfalls causing under- or overestimation. The paper gives practical guidelines and hints as to how to avoid some of these, particularly errors due to overlooked threshold stimulation and to unrecognized direct muscle fiber stimulation.