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W Metzner

Publications and source records attributed to W Metzner.

At least 19 recordsLinked to original sources
PubMed2000

Robustness and variability of neuronal coding by amplitude-sensitive afferents in the weakly electric fish eigenmannia.

We investigated the variability of P-receptor afferent spike trains in the weakly electric fish, Eigenmannia, to repeated presentations of random electric field AMs (RAMs) and quantified its impact on the encoding of time-varying stimuli. A new measure of spike timing jitter was developed using the notion of spike train distances recently introduced by Victor and Purpura. This measure of variability is widely applicable to neuronal responses, irrespective of the type of stimuli used (deterministic vs. random) or the reliability of the recorded spike trains. In our data, the mean spike count and its variance measured in short time windows were poorly correlated with the reliability of P-receptor afferent spike trains, implying that such measures provide unreliable indices of trial-to-trial variability. P-receptor afferent spike trains were considerably less variable than those of Poisson model neurons. The average timing jitter of spikes lay within 1-2 cycles of the electric organ discharge (EOD). At low, but not at high firing rates, the timing jitter was dependent on the cutoff frequency of the stimulus and, to a lesser extent, on its contrast. When spikes were artificially manipulated to increase jitter, information conveyed by P-receptor afferents was degraded only for average jitters considerably larger than those observed experimentally. This suggests that the intrinsic variability of single spike trains lies outside of the range where it might degrade the information conveyed, yet still allows for improvement in coding by averaging across multiple afferent fibers. Our results were summarized in a phenomenological model of P-receptor afferents, incorporating both their linear transfer properties and the variability of their spike trains. This model complements an earlier one proposed by Nelson et al. for P-receptor afferents of Apteronotus. Because of their relatively high precision with respect to the EOD cycle frequency, P-receptor afferent spike trains possess the temporal resolution necessary to support coincidence detection operations at the next stage in the amplitude-coding pathway.

Action Potentials↗
PubMed1999

Encoding and processing of sensory information in neuronal spike trains

Recently, a statistical signal-processing technique has allowed the information carried by single spike trains of sensory neurons on time-varying stimuli to be characterized quantitatively in a variety of preparations. In weakly electric fish, its application to first-order sensory neurons encoding electric field amplitude (P-receptor afferents) showed that they convey accurate information on temporal modulations in a behaviorally relevant frequency range (<80 Hz). At the next stage of the electrosensory pathway (the electrosensory lateral line lobe, ELL), the information sampled by first-order neurons is used to extract upstrokes and downstrokes in the amplitude modulation waveform. By using signal-detection techniques, we determined that these temporal features are explicitly represented by short spike bursts of second-order neurons (ELL pyramidal cells). Our results suggest that the biophysical mechanism underlying this computation is of dendritic origin. We also investigated the accuracy with which upstrokes and downstrokes are encoded across two of the three somatotopic body maps of the ELL (centromedial and lateral). Pyramidal cells of the centromedial map, in particular I-cells, encode up- and downstrokes more reliably than those of the lateral map. This result correlates well with the significance of these temporal features for a particular behavior (the jamming avoidance response) as assessed by lesion experiments of the centromedial map.

Journal Article↗
PubMed1999

Neural circuitry for communication and jamming avoidance in gymnotiform electric fish.

Over the past decade, research on the neural basis of communication and jamming avoidance in gymnotiform electric fish has concentrated on comparative studies of the premotor control of these behaviors, on the sensory processing of communication signals and on their control through the endocrine system, and tackled the question of the degree to which these behaviors share neural elements in the sensory-motor command chain by which they are controlled. From this wealth of investigations, we learned, first, how several segregated premotor pathways controlling a single central pattern generator, the medullary pacemaker nucleus, can provide a large repertoire of behaviorally relevant motor patterns. The results suggest that even small evolutionary modifications in the premotor circuitry can yield extensive changes in the behavioral output. Second, we have gained some insight into the concerted action of the brainstem, the diencephalon and the long-neglected forebrain in sensory processing and premotor control of communication behavior. Finally, these studies shed some light on the behavioral significance of multiple sensory brain maps in the electrosensory lateral line lobe that long have been a mystery. From these latter findings, it is tempting to interpret the information processing in the electrosensory system as a first step in the evolution towards the 'distributed hierarchical' organization commonly realized in sensory systems of higher vertebrates.

Animal Communication↗
PubMed1998

Segregation of behavior-specific synaptic inputs to a vertebrate neuronal oscillator.

Although essential for understanding the mechanisms underlying sensorimotor integration and motor control of behaviors, very little is known about the degree to which different behaviors share neural elements of the sensorimotor command chain by which they are controlled. Here, we provide, to our knowledge, the first direct physiological evidence that various modulatory premotor inputs to a vertebrate central pattern generator, the pacemaker nucleus in gymnotiform electric fish, carrying distinctly different behavioral information, can remain segregated from their various sites of origin in the diencephalon to the synaptic termination sites on different target neurons in the medullary pacemaker nucleus. During pharmacological activation of each of the premotor inputs originating from the three prepacemaker nuclei so far identified, we determined in vivo the changes in input resistance in the neuronal elements of the pacemaker nucleus, i.e., relay cells and pacemaker cells. We found that each input yields significantly different effects on these cells; the inputs from the two diencephalic prepacemaker nuclei, PPnC and PPnG, which resulted in increased oscillator activity, caused significantly lower input resistances in relay and pacemaker cells, respectively, exhibiting drastically different time courses. The input from the sublemniscal prepacemaker nucleus, which resulted in reduced oscillator activity, however, caused a significant increase in input resistance only in relay cells. Considering that the sensory pathways processing stimuli yielding these behaviors are separated as well, this study indicates that sensorimotor control of different behaviors can occur in strictly segregated channels from the sensory input of the brain all through to the synaptic input level of the final premotor command nucleus.

Animals↗
PubMed1998

Feature extraction by burst-like spike patterns in multiple sensory maps.

In most sensory systems, higher order central neurons extract those stimulus features from the sensory periphery that are behaviorally relevant (e.g.,Marr, 1982; Heiligenberg, 1991). Recent studies have quantified the time-varying information carried by spike trains of sensory neurons in various systems using stimulus estimation methods (Bialek et al., 1991; Wessel et al., 1996). Here, we address the question of how this information is transferred from the sensory neuron level to higher order neurons across multiple sensory maps by using the electrosensory system in weakly electric fish as a model. To determine how electric field amplitude modulations are temporally encoded and processed at two subsequent stages of the amplitude coding pathway, we recorded the responses of P-type afferents and E- and I-type pyramidal cells in the electrosensory lateral line lobe (ELL) to random distortions of a mimic of the fish's own electric field. Cells in two of the three somatotopically organized ELL maps were studied (centromedial and lateral) (Maler, 1979; Carr and Maler, 1986). Linear and second order nonlinear stimulus estimation methods indicated that in contrast to P-receptor afferents, pyramidal cells did not reliably encode time-varying information about any function of the stimulus obtained by linear filtering and half-wave rectification. Two pattern classifiers were applied to discriminate stimulus waveforms preceding the occurrence or nonoccurrence of pyramidal cell spikes in response to the stimulus. These signal-detection methods revealed that pyramidal cells reliably encoded the presence of upstrokes and downstrokes in random amplitude modulations by short bursts of spikes. Furthermore, among the different cell types in the ELL, I-type pyramidal cells in the centromedial map performed a better pattern-recognition task than those in the lateral map and than E-type pyramidal cells in either map.

Action Potentials↗
PubMed1997

A sensory brain map for each behavior?

Multiple brain maps are commonly found in virtually every vertebrate sensory system. Although their functional significance is generally relatively little understood, they seem to specialize in processing distinct sensory parameters. Nevertheless, to yield the stimulus features that ultimately elicit the adaptive behavior, it appears that information streams have to be combined across maps. Results from current lesion experiments in the electrosensory system, however, suggest an alternative possibility. Inactivations of different maps of the first-order electrosensory nucleus in electric fish, the electrosensory lateral line lobe, resulted in markedly different behavioral deficits. The centromedial map is both necessary and sufficient for a particular electrolocation behavior, the jamming avoidance response, whereas it does not affect the communicative response to external electric signals. Conversely, the lateral map does not affect the jamming avoidance response but is necessary and sufficient to evoke communication behavior. Because the premotor pathways controlling the two behaviors in these fish appear to be separated as well, this system illustrates that sensory-motor control of different behaviors can occur in strictly segregated channels from the sensory input of the brain all through to its motor output. This might reflect an early evolutionary stage where multiplication of brain maps can satisfy the demand on processing a wider range of sensory signals ensuing from an enlarged behavioral repertoire, and bridging across maps is not yet required.

Animals↗
PubMed1997

A method to biotinylate and histochemically visualize ibotenic acid for pharmacological inactivation studies.

Ibotenic acid (IA) and kainic acid (KA) are commonly used tools to selectively inactivate neuronal perikarya, eventually leading to their degeneration, without affecting fibers of passage. Reversible inactivations and experimental paradigms that do not allow for long survival times, however, do not permit for histological verification of the site and extent of the lesion by identifying the area showing gliosis. We describe here a method in which IA and KA were conjugated with biotin and thus could be easily visualized histochemically. We pressure-injected biotinylated IA and KA into various hindbrain areas of the electrosensory system in electric fish while monitoring neuronal responses at the injection site and assessing effects on the behavior. Whereas the effects of biotinylated IA did not differ from those of the unbiotinylated form, biotinylated KA lost its physiological activity. Thus, only biotinylated IA could be used successfully. The size of the gliosis seen after a survival time of seven days was similar to the extent of biotin label observed after injection of comparable volumes of biotinylated IA. Moreover, this method resulted in labeling of individual neurons presumably affected by IA and yielded information about their projection patterns which was comparable to labeling seen after intracellular injections of neurobiotin or biocytin.

Animals↗
PubMed1996

From stimulus encoding to feature extraction in weakly electric fish.

Animals acquire information about sensory stimuli around them and encode it using an analogue or a pulse-based code. Behaviourally relevant features need to be extracted from this representation for further processing. In the electrosensory system of weakly electric fish, single P-type electroreceptor afferents accurately encode the time course of random modulations in electric-field amplitude. We applied a stimulus estimation method and a signal-detection method to both P-receptor afferents and their targets, the pyramidal cells in the electrosensory lateral-line lobe. We found that although pyramidal cells do not accurately convey detailed information about the time course of the stimulus, they reliably encode up- and downstrokes of random modulations in electric-field amplitude. The presence of such temporal features is best signalled by short bursts of spikes, probably caused by dendritic processing, rather than by isolated spikes. Furthermore, pyramidal cells outperform P-receptor afferents in signalling the presence of temporal features in the stimulus waveform. We conclude that the sensory neurons are specialized to acquire information accurately with little processing, whereas the following stage extracts behaviourally relevant features, thus performing a nonlinear pattern-recognition task.

Action Potentials↗
PubMed1996

Anatomical basis for audio-vocal integration in echolocating horseshoe bats.

Neurophysiological recordings suggest that audio-vocal neurons located in the paralemniscal tegmentum of the midbrain in horseshoe bats provide an interface between the pathways for auditory sensory processing and those for the motor control of vocalization. To verify these physiological results anatomically, the projection pattern of the audio-vocally active area in the paralemniscal tegmentum was investigated by using extracellular tracer injections of wheat germ agglutinin conjugated to horseradish peroxidase. Several nuclei of the lemniscal auditory pathway (dorsal nucleus of the lateral lemniscus, central nucleus of the inferior colliculus, lateral superior olive) as well as the nucleus of the central acoustic tract appear to project to the paralemniscal tegmentum. Other possible sources of afferent projections are a small but distinctly labeled structure within the lateral hypothalamic area, the substantia nigra pars compacta, the deep mesencephalic nucleus, the rostral portion of the inferior colliculus, the deep and intermediate layers of the superior colliculus, and several small areas in the rhombencephalic reticular formation. No direct efferent projection from the audio-vocally active area of the paralemniscal tegmentum to primarily auditory structures was found. Instead, the main targets were structures that are involved in the control of different motor patterns. These targets include the deep and intermediate layers of the superior colliculus and the dorsomedial portion of the facial nucleus, both of which most probably control pinna movements in cats, and the reticular formation medial and caudal to the facial nucleus and rostral to the nucleus ambiguus, which represents an area involved in the control of vocalization. Hence, the anatomical projection pattern suggests that the paralemniscal tegmentum in horseshoe bats serves as a link between the processing of auditory information and the control of vocalization and related motor patterns.

Animals↗
PubMed1996

Motor control of the jamming avoidance response of Apteronotus leptorhynchus: evolutionary changes of a behavior and its neuronal substrates.

The two closely related gymnotiform fishes, Apteronotus and Eigenmannia, share many similar communication and electrolocation behaviors that require modulation of the frequency of their electric organ discharges. The premotor linkages between their electrosensory system and their medullary pacemaker nucleus, which controls the repetition rate of their electric organ discharges, appear to function differently, however. In the context of the jamming avoidance response, Eigenmannia can raise or lower its electric organ discharge frequency from its resting level. A normally quiescent input from the diencephalic pre-pacemaker nucleus can be recruited to raise the electric organ discharge frequency above the resting level. Another normally active input, from the sublemniscal pre-pacemaker nucleus, can be inhibited to lower the electric organ discharge frequency below the resting level (Metzner 1993). In contrast, during a jamming avoidance response, Apteronotus cannot lower its electric organ discharge frequency below the resting level. The sublemniscal pre-pacemaker is normally completely inhibited and release of this inhibition allows the electric organ discharge frequency to rise during the jamming avoidance response. Further inhibition of this nucleus cannot lower the electric organ discharge frequency below the resting level. Lesions of the diencephalic pre-pacemaker do not affect performance of the jamming avoidance response. Thus, in Apteronotus, the sublemniscal pre-pacemaker alone controls the changes of the electric organ discharge frequency during the jamming avoidance response.

Animals↗
PubMed1993

The jamming avoidance response in Eigenmannia is controlled by two separate motor pathways.

The gymnotiform fish Eigenmannia generates weakly electric signals for electrolocation and communication. The signals are produced by electric organ discharges (EODs) that are driven by a medullary pacemaker nucleus. To avoid jamming by neighboring conspecifics with similar frequencies, a fish raises its own EOD frequency if the neighbor's frequency is lower, and it lowers its EOD frequency if the neighbor's frequency is higher (Watanabe and Takeda, 1963). Both the raising and lowering of EOD frequency of this jamming avoidance response (JAR; Bullock et al., 1972) are thought to be controlled by feature-extracting neurons in the diencephalic prepacemaker nucleus (PPn-G) that discriminate the sign of the frequency difference between the jamming signal and the fish's EOD (Kawasaki et al., 1988a; Rose et al., 1988; for review, see Heiligenberg, 1991). These prepacemaker neurons are excited in response to lower jamming frequencies, thereby raising the frequency, and inhibited by higher jamming frequencies, producing a discharge deceleration. The results of experiments presented here, however, suggest a mechanism for the motor control of the JAR that is different from the one described previously (see, e.g., Heiligenberg, 1991). Two prepacemaker nuclei, one PPn-G and one sublemniscal prepacemaker nucleus (SPPn) (Keller et al., 1991 a,b), which provide the only known inputs to the pacemaker, were lesioned selectively. This article explores the effects of these lesions on the JAR. Pharmacological experiments were used to elucidate the transmitter types involved. The results suggest that the JAR is controlled by two separate motor pathways. One controls frequency rises and originates in the dorsal substructure of the nucleus electrosensorius (Keller, 1988). It sends excitatory connections to the diencephalic prepacemaker and finally to the pacemaker nucleus, where AMPA-type receptors mediate the synaptic transmission. The second pathway controls frequency decreases and originates in the ventral substructure of the nucleus electrosensorius. It provides GABAergic input to the SPPn. The SPPn is tonically active and also controls the EOD frequency even in the absence of jamming signals. Its projection to the pacemaker nucleus is mediated by NMDA-type receptors. The results of this study suggest that there is no single population of final, feature-extracting elements or "recognition units" that controls JAR-related shifts of the pacemaker frequency. Instead, the motor control of the JAR consists of an interaction of two independent pathways according to a "push-pull" principle.

Animals↗
PubMed1993

An audio-vocal interface in echolocating horseshoe bats.

The control of vocalization depends significantly on auditory feedback in any species of mammals. Echolocating horseshoe bats, however, provide an excellent model system to study audio-vocal (AV) interactions. These bats can precisely control the frequency of their echolocation calls by monitoring the characteristics of the returning echo; they compensate for flight-induced Doppler shifts in the echo frequency by lowering the frequency of the subsequent vocalization cells (Schnitzler, 1968; Schuller et al., 1974, 1975). It was the aim of this study to investigate the neuronal mechanisms underlying this Doppler-shift compensation (DSC) behavior. For that purpose, the neuronal activity of single units was studied during spontaneous vocalizations of the bats and compared with responses to auditory stimuli such as playback vocalizations and artificially generated acoustic stimuli. The natural echolocation situation was simulated by triggering an acoustic stimulus to the bat's own vocalization and by varying the time delay of this artificial "echo" relative to the vocalization onset. Single-unit activity was observed before, during, and/or after the bat's vocalization as well as in response to auditory stimuli. However, the activity patterns associated with vocalization differed from those triggered by auditory stimuli even when the auditory stimuli were acoustically identical to the bat's vocalization. These neurons were called AV neurons. Their distribution was restricted to an area in the paralemniscal tegmentum of the midbrain. When the natural echolocation situation was stimulated, the responses of AV neurons depended on the time delay between the onset of vocalization and the beginning of the simulated echo. This delay sensitivity disappeared completely when the act of vocalization was replaced by an auditory stimulus that mimicked acoustic self-stimulation during the emission of an echolocation call. The activity of paralemniscal neurons was correlated with all parameters of echolocation calls and echoes that are relevant in context with DSC. These results suggest a model for the regulation of vocalization frequencies by inhibitory auditory feedback.

Adaptation, Physiological↗