Biomedical subjects

W Heiligenberg

Publications and source records attributed to W Heiligenberg.

At least 37 records · Page 2Linked to original sources

PubMed1989

Development of the electrosensory nervous system in Eigenmannia (Gymnotiformes): I. The peripheral nervous system.

The nerves of the anterior lateral line system in embryonic and larval stages of the weakly electric gymnotiform fish Eigenmannia were visualized by injection of the fluorescent marker DiI into the primordium of the anterior (ALLN) and posterior (PLLN) lateral line nerves. Examination of developmental series reveals that the nerve fibers that innervate the electrosensory and mechanosensory components of the anterior lateral line system are present before the first mechanoreceptors and electroreceptors have differentiated. This suggests that nerve fibers might induce the formation of lateral line receptors. Whereas the innervation of the mechanoreceptive system is already established at an early stage, the afferent innervation of electroreceptors continues to arborize in the periphery, presumably by following pioneer axon pathways. The earliest recognizable stage of the anterior lateral line nerve ganglion (ALLNG) is evident 2 days after spawning. The ganglion shows two germinal cell masses that develop into the supraorbital-infraorbital and the hyomandibular placodes. The supraorbital-infraorbital placode forms the dorsal part of the ALLNG; the hyomandibular placode forms the ventral part of the ALLNG. Counts of ALLNG cells in embryonic, larval, and adult stages of Eigenmannia show that, at each stage examined, the number of ganglion cells is always significantly larger than the number of mechanoreceptors and electroreceptor units in the periphery. During development, the distribution of ALLNG cell diameters shifts from a unimodal distribution in juveniles to a bimodal distribution in adults, peaking at 8 microns and 18 microns. These results suggest that tuberous electroreceptive organs, which are innervated by the large ALLNG cells, may not be functional prior to day 18. Our results further suggest that the number of ALLNG cells correlates with the rate of induction of lateral line receptors in the periphery.

Animals↗

PubMed1989

HRP labeling and ultrastructural localization of prepacemaker terminals within the medullary pacemaker nucleus of the weakly electric gymnotiform fish Apteronotus leptorhynchus.

The prepacemaker nucleus (PPN) in the midbrain of gymnotiform electric fish projects to the pacemaker nucleus (PN) in the medulla and modulates its rhythmic discharges in the context of social electric communication. Anterograde labeling of PPN axons with HRP and ultrastructural studies of their terminations in the PN have shown that PPN neurons form synaptic contacts with both types of neurons in the PN, pacemaker cells, and relay cells.

Animals↗

PubMed1989

Distinct mechanisms of modulation in a neuronal oscillator generate different social signals in the electric fish Hypopomus.

The medullary pacemaker nucleus of the gymnotiform electric fish, Hypopomus, is a relatively simple neuronal oscillator which contains pacemaker cells and relay cells. The pacemaker cells generate a regular discharge cycle and drive the relay cells which trigger pulse-like electric organ discharges (EODs). The diencephalic prepacemaker nucleus (PPN) projects to the pacemaker nucleus and modulates its activity to generate a variety of specific discharge patterns which serve as communicatory signals (Figs. 2 and 3). While inducing such signals by microiontophoresis of L-glutamate to the region of the PPN (Fig. 4) of curarized animals, we monitored the activity of neurons in the pacemaker nucleus intracellularly. We found that pacemaker cells and relay cells were affected differently in a manner specific to the type of EOD modulation (Figs. 5-10). The normal sequence of pacemaker cell and relay cell firing was maintained during gradual rises and falls in discharge rate. Both types of cells ceased to fire during interruptions following a decline in discharge rate. During sudden interruptions, however, relay cells were steadily depolarized, while pacemaker cells continued to fire regularly. Short and rapid barrages of EODs, called "chirps", were generated through direct and synchronous activation of the relay cells whose action potentials invaded pacemaker cells antidromically and interfered with their otherwise regular firing pattern.

Action Potentials↗

PubMed1989

From distributed sensory processing to discrete motor representations in the diencephalon of the electric fish, Eigenmannia.

During their jamming avoidance response (JAR), weakly electric fish of the genus Eigenmannia shift their electric organ discharge (EOD) frequency away from a similar EOD frequency of a neighboring fish. The behavioral rules and neural substrates for stimulus recognition and motor control of the JAR have been extensively studied (see review by Heiligenberg 1986). The diencephalic nucleus electrosensorius (nE) links sensory processing within the torus semicircularis and optic tectum with the mesencephalic prepacemaker nucleus which, in turn, modulates the medullary pacemaker nucleus and hence the EOD frequency. Two separate areas within the nE responsible for JAR-related EOD frequency rises and frequency falls, respectively, were identified by iontophoresis of the excitatory amino acid L-glutamate. Bilateral lesion of the areas causing EOD frequency rises resulted in elimination of JAR-related frequency rises above a baseline frequency obtained in the absence of a jamming stimulus. Similarly, bilateral lesion of the areas causing frequency falls resulted in a loss of JAR-related frequency falls below the baseline frequency. Whether these areas are also responsible for non-JAR-related frequency shifts is not known. The strength of response and spatial extent of the areas causing frequency shifts varied among fish and also varied in individual fish, reflecting the strength of JAR-related frequency shifts and the balance of activities in frequency-rise and frequency-fall areas. Local application of bicuculline-methiodide or GABA demonstrated a tonic inhibitory input to each area and suggests a reciprocal inhibitory interaction between the two ipsilateral areas, possibly accounting for much of the individual plasticity. The nE thus is a site for neuronal transformation from distributed, topographically organized processing within the laminated structures of the torus and tectum to discrete cell clusters which control antagonistic motor responses.

Action Potentials↗

PubMed1989

Different classes of glutamate receptors mediate distinct behaviors in a single brainstem nucleus.

We have taken advantage of the increasing understanding of glutamate neuropharmacology to probe mechanisms of well-defined vertebrate behaviors. Here we report a set of experiments that suggests distinct roles for two major classes of glutamate receptors in a discrete premotor nucleus of the brainstem. The medullary pacemaker nucleus of weakly electric fish is an endogenous oscillator that controls the electric organ discharge (EOD). Its regular frequency of firing is modulated during several distinct behaviors. The pacemaker nucleus continues firing regularly when isolated in vitro, and modulatory behaviors can be reproduced by stimulating the descending input pathway. Glutamate agonists applied to the pacemaker in vitro produced increases in frequency, while glutamate antagonists selectively blocked stimulus-induced modulations. Experiments with glutamate antagonists in the intact animal resulted in specific effects on two well-characterized behaviors. Our data indicate that these behaviors are separately mediated in the pacemaker by receptors displaying characteristics of the kainate/quisqualate and N-methyl-D-aspartate subtypes of glutamate receptor, respectively.

2-Amino-5-phosphonovalerate↗

PubMed1989

Coding and processing of electrosensory information in gymnotiform fish.

Studies of the electrosensory system of gymnotiform fish have revealed principles of neuronal coding and processing of information which also characterize more advanced systems, such as vision and audition in higher vertebrates. 1. Animals may have different classes of receptors adapted to code different variables within a given modality, and the separation of their central projections provides the basis for independent initial processing of these variables by higher-order neurones. 2. These separate pathways, however, eventually converge at the level of still higher-order neurones which are adapted to 'recognize' particular spatial and temporal constellations, or patterns, of the stimulus variables conveyed by these pathways. 3. As different stimulus patterns may control different forms of behavioural responses, corresponding neuronal structures can be identified which are adapted to recognize specific patterns. Neurones at an early level of pattern discrimination may still show very general response properties, whereas neurones closer to the ultimate control of a given behaviour show more specific response properties. These latter are less sensitive to stimulus features which are irrelevant to the control of the behaviour, and they code relevant features more purely and with higher acuity than do lower-level neurones. 4. The acuity of stimulus discrimination displayed by some high-order neurones may rival that observed at the behavioural level. This high sensitivity is achieved through pooling and integration of information supplied by large populations of less-sensitive receptors and lower-order neurones.

Afferent Pathways↗

PubMed1989

Sexual maturity-dependent changes in neuronal morphology in the prepacemaker nucleus of adult weakly electric knifefish, Eigenmannia.

Knifefish of the genus Eigenmannia (Gymnotiformes, Teleostei) are seasonal breeders that spawn only during the tropical rainy season. Both sexes modulate their otherwise constant wave-like electric organ discharges (EODs) in the context of courtship and aggressive behavior by "chirps," abrupt frequency modulations with brief interruptions. Play-backs of recordings of male courtship chirps can induce spawning in gravid females (Hagedorn and Heiligenberg, 1985). The EOD, produced by a specialized electric organ, is under the control of a pacemaker nucleus (Pn) in the medulla oblongata. Injections of HRP into the Pn label only a small cluster of cells bilaterally at the boundary of diencephalon and mesencephalon, constituting the prepacemaker nucleus, PPn (Heiligenberg et al., 1981). Microstimulation experiments have shown that chirp-like EOD modulations can be elicited from a subnucleus of the PPn, the PPn-C (Kawasaki and Heiligenberg, 1988; Kawasaki et al., 1988). By retrograde HRP labeling, we investigated the dependence of the PPn's morphology upon the sexual maturity of the fish. The most prominent effect was that, during the breeding season, females developed an abundance of "varicosities," swellings 1-4 microns in diameter in distal regions of dendrites at a density of approximately 1/10 microns. In contrast to mature females, immature females had none or only a few varicosities. Such a clear correlation between the abundance of varicosities and relative gonadal weight was not found in males, most likely because testicular and dendritic development are not strictly synchronized. After the onset of the simulated dry season, however, relative gonadal weight, as well as the number of varicosities, was reduced drastically in both sexes. This reduction in the number of varicosities is accompanied by a decrease in their diameter. Varicosities may represent growing buds or regions of synaptic input from afferent areas or both. Reconstruction of individual PPn-C neurons showed maturity-dependent changes in the pattern of dendritic proliferation in females. Such dynamic changes in the structure of neurons might subserve seasonal modifications in an animal's propensity to execute specific behaviors.

Animals↗

PubMed1988

Temporal hyperacuity in single neurons of electric fish.

Behavioural studies have revealed that animals can resolve temporal disparities in the microsecond range. This resolution is far superior to that of individual receptors, and it must therefore be achieved through central neuronal mechanisms. It is unclear, however, whether such sensitivity ever emerges at the level of single neurons, or whether it is apparent only at the behavioural level through the collective action of many less-sensitive neurons. We have found that single neurons in the pre-pacemaker nucleus of a weakly electric fish are sensitive to temporal disparities as small as 1 microsecond, the highest temporal sensitivity ever observed at the single-neuron level. The remarkable temporal resolution of these pre-pacemaker neurons results from a high degree of spatial convergence of afferent inputs. These neurons represent the final elements of a sensory hierarchy and directly control the jamming avoidance response by which these fish regulate the frequency of their electric organ discharges.

Animals↗

PubMed1988

Anatomical and functional organization of the prepacemaker nucleus in gymnotiform electric fish: the accommodation of two behaviors in one nucleus.

The diencephalic prepacemaker nucleus (PPn) of gymnotiform electric fish projects to the medullary pacemaker nucleus and modulates its regular firing frequency. Each firing of the pacemaker, in turn, drives an electric organ discharge (EOD). Two types of PPn neurons were retrogradely labeled from the pacemaker with HRP in Eigenmannia and Apteronotus. In both species, smaller ovoidal cells were found in the dorsomedial part of the PPn (PPn-G), and larger multipolar cells were found in the ventrolateral part of the PPn (PPn-C). This morphological distinction between the two subnuclei in the PPn was paralleled by a functional dichotomy. Microiontophoresis of L-glutamate in the PPn-G of both species elicited slow and gradual accelerations of EOD frequency characterized by a time constant on the order of seconds. The elicited frequency modulations were similar to those observed during the jamming avoidance response and during courtship. Glutamate stimulation of the PPn-C, in contrast, produced fast and abrupt frequency modulations characterized by a time constant on the order of milliseconds. These abrupt modulations resembled "chirps" observed during courtship and aggression. Similar behavior was produced by intracellular current injection into a PPn-C neuron of Apteronotus, and intracellular labeling of this neuron with Lucifer Yellow revealed a multipolar PPn-C neuron similar to those retrogradely labeled with HRP.

Action Potentials↗

PubMed1988

How sensory maps could enhance resolution through ordered arrangements of broadly tuned receivers.

We investigate the properties of a model recently introduced by Heiligenberg (1987) for an array of sensors tuned to progressively higher ranges of a continuous stimulus variable x and with bell shaped single response curve with width parameter d. The main result is that as d increases, the overall response rapidly becomes almost linear in a very smooth and robust fashion. Biological relevance and implications of the model and of its extensions are discussed together with a few examples.

Mathematics↗

PubMed1988

'Recognition units' at the top of a neuronal hierarchy? Prepacemaker neurons in Eigenmannia code the sign of frequency differences unambiguously.

The electric fish, Eigenmannia, is able to discriminate the sign of the frequency difference, Df, between a neighbor's electric organ discharges (EODs) and its own. The fish lowers its EOD frequency for positive Dfs and raises its frequency for negative Dfs to minimize jamming of its electrolocation ability by a neighbor's EODs of similar frequency. This jamming avoidance response (JAR) is controlled by a group of 'sign-selective' neurons in the prepacemaker nucleus (PPN) that is located at the boundary of the midbrain and the diencephalon (Fig. 1). Extracellular recordings from a total of 35 neurons revealed a great similarity between behavioral and neuronal response properties: 1. All neurons fired vigorously for negative Dfs and were almost silent for positive Dfs, regardless of the orientation of the jamming stimulus, and thus discriminated the sign of Df unambiguously (Fig. 2). 2. In accordance with behavioral observations, individual neurons failed to discriminate the sign of Df when the jamming stimulus had the same field geometry as the signal mimicking the animal's own EOD (Fig. 3). 3. Df magnitudes which evoke strongest JARs, usually 4 to 8 Hz, also induced most vigorous responses in sign-selective neurons (Fig. 5). 4. Behavioral and neuronal thresholds for the detection of small jamming signals were similar. Threshold for sign selectivity was reached when the amplitude ratio of the jamming signal to the EOD mimic, measured near the head surface, was 0.001. This value corresponds to a maximal temporal disparity (a necessary cue for performing a correct JAR) of 1 to 2 microseconds for signals received by the two sides of the body in a transverse jamming field (Fig. 7). 5. The effects of two jamming fields, offered orthogonally to each other, may interact nonlinearly at the behavioral as well as at the neuronal level. A positive Df presented in one field may suppress behavioral and neuronal responses to modulations of the sign of Df in the other field (Fig. 8c).

Animals↗

PubMed1988

Individual prepacemaker neurons can modulate the pacemaker cycle of the gymnotiform electric fish, Eigenmannia.

The prepacemaker nucleus (PPN) in the midbrain of the gymnotiform electric fish Eigenmannia provides the only known neuronal input to the medullary pacemaker nucleus, which triggers each electric organ discharge (EOD) cycle by a single command pulse. Electrical stimulation of the PPN elicited two distinct forms of modulations in the pacemaker activity, brief accelerations, hence referred to as 'chirps', and gradual frequency shifts with a time constant of approximately one second. The associated EOD modulations were indistinguishable from natural communication signals. Depending upon the site of stimulation, the two forms of modulation could be elicited alone or superimposed (Fig. 1). Stimulation sites eliciting only chirps could be separated from sites eliciting only gradual shifts by as little as 60 micron. The magnitude of the elicited chirps depended upon the timing of the pulse stimulus with reference to the phase of the pacemaker cycle (Figs. 2, 3). Extracellular and intracellular recordings of single PPN neurons revealed that an action potential from a single neuron generates a chirp, and that the magnitude of the chirp depends upon the timing of the action potential with reference to the phase of the pacemaker cycle (Figs. 4, 5). The spike activity of these neurons had no relation to the jamming avoidance response (JAR), suggesting independent neuronal mechanisms for chirps and the JAR. Depolarization of such neurons by current injection produced bursts of chirps (Fig. 6), and intracellular injection of Lucifer Yellow identified these cells as a large type of PPN neuron which could also be retrogradely labeled from the pacemaker with horseradish peroxidase (HRP) (Fig. 7).(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗

PubMed1988

Electrosensory maps form a substrate for the distributed and parallel control of behavioral responses in weakly electric fish.

Electroreceptors, distributed over the body surface of weakly electric fish, code the local amplitude and phase, or timing of zerocrossing, of the animal's electric signals. These signals are generated by rhythmic discharges of the electric organ and form a dipole-like field around the animal. This field is perturbed by interference with electric fields of other fish as well as by the appearance of objects electrically different from water. The spatial and temporal structure of such perturbations can be interpreted as the electric image of interfering fields and moving objects. This strategy of assessing the environment is called 'electrolocation', a form of 'seeing' with the body surface. Electric images are analyzed in somatotopically ordered strata of neurons within the central nervous system. Primary electrosensory afferents project to somatotopically ordered layers of higher-order neurons in the electrosensory lateral line lobe (ELL) of the hindbrain. Phase and amplitude information are processed in separate layers of the ELL. The phase of the signal in a given region of the body surface is coded by the timing of spikes of spherical cells marking the zerocrossings of the electric signal. This phase information is relayed to lamina 6 of the torus semicircularis of the midbrain. Rises and falls in local amplitude are coded by the activity of different pyramidal cell types, E- and I-units, which project to various laminae of the torus above and below lamina 6. The somatotopic organization of the torus allows for computations of spatial patterns in electrosensory information. Within lamina 6, differences in the phase of signals from different parts of the body surface are computed. Differential-phase information is then relayed to deeper laminae of the torus and remains in topographic register with amplitude information. This organization allows for joint evaluation of spatially related patterns of amplitude and phase modulations on the animal's body surface within local neuronal circuits of the torus. A topographic projection of the torus relays amplitude and differential-phase information to the optic tectum where a further joint evaluation of amplitude and phase serves to control behavioral responses. The control of a particular behavioral performance, the 'jamming avoidance response', is of a distributed nature in that the representations of individual sites on the body surface contribute cumulatively to shift the electric organ pacemaker frequency.(ABSTRACT TRUNCATED AT 400 WORDS)

Action Potentials↗

PubMed1988

The development of the jamming avoidance response in the weakly electric fish, Eigenmannia.

The jamming avoidance response (JAR) in young weakly electric fish, Eigenmannia, develops at the onset of a functional electrosensory phase-coding system, a neural pathway that is critical for the performance of the JAR. Size (measured in head to tail length) seems to be the best predictor of the onset of the JAR. A distinguishable JAR value (0.15 Hz or greater) develops in fish at a length of 12-15 mm, and its strength continues to increase with maturity until it approaches an adult value (8-20 Hz) at a length of about 45 mm. The JAR is not dependent upon social interactions, as it can be performed correctly upon first stimulation by animals raised in individual aquaria from the egg stage. Preliminary studies suggest that there are anatomical correlates to the development of the JAR behavior. As the JAR strengthens with age, there is a concomitant increase in the number of giant cells and a development of the commissural plexus in lamina 6 of the torus semicircularis. Giant cells play a pivotal role in the phase comparison circuit. Both phase and amplitude information play a role in the proper performance of the JAR, but the discrete nature of the phase comparison circuit allows the correlation between the development of the JAR and an essential part of the phase comparison circuit (lamina 6 of the torus) to be observed in Eigenmannia.

Animals↗

PubMed1987

Ultrastructural studies of physiologically identified electrosensory afferent synapses in the gymnotiform fish, Eigenmannia.

Eigenmannia is a weakly electric fish that emits a constant-frequency electric organ discharge (EOD). Probability coder (P unit) and phase coder (T unit) electroreceptive afferents differentially encode changes in EOD amplitude and phase, respectively. physiologically identified T and P units were intracellularly labelled with HRP and their terminals were examined with electron microscopy to determine their postsynaptic targets. This technique reveals that phase and amplitude are relayed to first-order electrosensory neurons by two parallel but not independent pathways. P-type afferents terminate on granular interneurons, basilar pyramidals, and polymorphic cells, electrosensory lateral line lobe targets that monitor amplitude modulations, but P-type afferents do not contact spherical cells. T-type afferents relay phase information to spherical cells and thus form a separate afferent pathway. T unit terminals do not synapse directly on basilar pyramidal cells. Collateral branches from T-type afferents, however, were also found to terminate on granule and polymorphic cells, thereby adding phase information into the amplitude channel. P- and T-type afferents exhibit cellular specificity by forming synaptic junctions with different subsets of post synaptic targets in the deep neuropil. The afferent terminals make either asymmetric chemical or gap junction synapses depending on the identity of the post synaptic target. T units contacting granule cells or polymorphic cells had not been previously described. Two possible roles of adding phase to amplitude information are discussed in terms of electrolocation.

Animals↗

PubMed1987

Central processing of sensory information in electric fish.

Comparative studies of neural mechanisms underlying the perception of natural stimulus patterns and the control of adaptive behavioral responses have revealed organizational principles that are shared by a wide spectrum of animals. Mechanisms of perception and motor control are commonly executed in a distributed network of neurons that lack 'pontifical' elements. Individual neurons even at an organizational level as high as the optic tectum may still have very general response characteristics, and the recruitment of individual neurons reveals little about the nature of the stimulus situation outside. Only the joint evaluation of messages from large populations of such neurons yields unambiguous pictures of the outside world. Stimulus variables are commonly mapped continuously within a stratum of neurons so that their variation over time can be monitored by mechanisms similar to motion detection in a retina. The ordered representation of a stimulus variable within an array of broadly tuned elements allows for a degree of stimulus resolution that by far exceeds that of individual elements in the array. Neural systems are burdened by their evolutionary history and suffer from imperfections that are overcome by a patchwork of compensations. The existence of multiple neuronal representations of sensory information and multiple circuits for the control of behavioral responses should provide the necessary freedom for evolutionary tinkering and the invention of new designs.

Animals↗

PubMed1987

'Ancestral' neural mechanisms of electrolocation suggest a substrate for the evolution of the jamming avoidance response.

The genus Sternopygus, believed to reflect ancestral traits of gymnotiform electric fish, is closely related to the more 'modern' genus Eigenmannia (Mago-Leccia 1978; Fink and Fink 1981). Sternopygus is the only known genus of electric fish that does not perform a jamming avoidance response (JAR) to minimize the potentially detrimental effects of signal interference between discharging neighbors (Bullock et al. 1972, 1975), and its ability to electrolocate objects is rather immune to jamming (Matsubara and Heiligenberg 1978). By studying the responses of midbrain neurons to stimulus regimes effective in eliciting the JAR in Eigenmannia, we found that Sternopygus has neurons capable of discriminating the sign of the difference frequency between interfering electric organ discharges (EODs). These 'sign-selective' neurons, which are believed to be important elements in the control of the JAR in Eigenmannia, may, therefore, fulfill a more general function in the detection of moving objects and conspecifics but could potentially be assembled for the evolution of a JAR in Sternopygus. The relative immunity to jamming in this genus may result, in part, from a stronger reliance upon the ampullary electrosensory system which operates in the DC and low-frequency range, outside the EOD spectrum of these fish.

Action Potentials↗

PubMed1987

Intracellular recording in the medullary pacemaker nucleus of the weakly electric fish, Apteronotus, during modulatory behaviors.

1. The weakly electric gymnotiform fish, Apteronotus leptorhynchus, can be induced to perform a variety of modulations of its quasi-sinusoidal, electric organ discharge (EOD) in acute physiological preparations. These modulations, many of which are communicatory in function, include the jamming avoidance response (JAR). We have recorded intracellularly from neurons of the medullary pacemaker nucleus which is responsible for maintaining the ongoing EOD frequency during these modulatory behaviors. 2. We have used dye-filled microelectrodes to characterize single cell morphology of the two types of cells in the pacemaker nucleus (relay and pacemaker cells) and to localize anatomically the site of the differing responses we see during frequency modulations. We have also recorded with KCl-filled electrodes and attributed these data to cell type and location on the basis of characteristic behavior during these modulations. 3. Much of our data deals with chirps, brief accelerations of the EOD frequency lasting 10 to 14 ms. We see distinct patterns of activity in the pacemaker nucleus corresponding to different anatomical locations: the relay cell soma and axon, and the pacemaker cell soma and axon. Most of these loci show a marked rise in baseline voltage during the acceleration in spike frequency. The most unusual of these is the pacemaker cell axon which displays an often extreme decline in spike amplitude concurrent with the chirp (Fig. 7A). 4. 'Yodeling' (Dye 1987) appears to involve similar, characteristic changes in the pattern of firing as those seen during chirping. Similar quantitative analyses suggest that the JAR involves a different mechanism, however.

Animals↗