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W Heiligenberg

Publications and source records attributed to W Heiligenberg.

At least 19 recordsLinked to original sources
PubMed1992

The structure of the diencephalic prepacemaker nucleus revisited: light microscopic and ultrastructural studies.

The prepacemaker nucleus (PPn), a bilateral cluster of neurons at the boundary of diencephalon and mesencephalon, controls frequency modulations of the electric organ discharge in weakly electric knifefish (Eigenmannia sp.). Previous light microscopic studies employing retrograde labelling with horseradish peroxidase suggested that the PPn is restricted to a small area, located approximately 400 microns laterally from the third ventricle and fusing at its medial edge with the thalamic central posterior nucleus (CP). In the present investigation we used Phaseolus vulgaris-leucoagglutinin and cholera toxin as highly sensitive markers. In contrast to the previous studies, these experiments yielded a large number of labelled cells not only in the region of the traditionally defined PPn but also in an area reaching far into the CP. Since the PPn has been defined by retrograde labelling rather than by topographic criteria, this result questions the traditional separation between PPn and CP. Such a notion is in agreement with observations of Nissl-stained sections at the light microscopic level and with a quantitative analysis of several morphological characteristics of the cell bodies in the PPn and CP at the ultrastructural level. Both sets of experiments failed to find differences between the two nuclei. Furthermore, autoradiographic studies have shown that, even in adulthood, cells are continuously born within the ventricular zone of the CP, and at least some of these newborn cells differentiate into CP cells and migrate laterally towards the PPn. Therefore, we postulate that CP and PPn form one large complex, with the medial CP providing precursors of neurons in the lateral CP and PPn.

Animals↗
PubMed1992

Development of the jamming avoidance response and its morphological correlates in the gymnotiform electric fish, Eigenmannia.

The electric fish, Eigenmannia, will smoothly shift the frequency of its electric organ discharge away from an interfering electric signal. This shift in frequency is called the jamming avoidance response (JAR). In this article, we analyze the behavioral development of the JAR and the anatomical development of structures critical for the performance of the JAR. The JAR first appears when juvenile Eigenmannia are approximately 1 month old, at a total length of 13-18 mm. We have found that the establishment of much of the sensory periphery and of central connections precedes the onset of the JAR. We describe three aspects of the behavioral development of the JAR: (a) the onset and development of the behavior is closely correlated with size, not age; (b) the magnitude (in Hz) of the JAR increases with size until the juveniles display values within the adult range (10-20 Hz) at a total length of 25-30 mm; and (3) the JAR does not require prior experience or exposure to electrical signals. Raised in total electrical isolation from the egg stage, animals tested at a total length of 25 mm performed a correct JAR when first exposed to the stimulus. We examine the development of anatomical areas important for the performance of the JAR: the peripheral electrosensory system (mechano- and electroreceptors and peripheral nerves); and central electrosensory pathways and nuclei [the electrosensory lateral line lobe (ELL), the lateral lemniscus, the torus semicircularis, and the pace-maker nucleus]. The first recognizable structures in the developing electrosensory system are the peripheral neurites of the anterior lateral line nerve. The afferent nerves are established by day 2, which is prior to the formation of receptors in the epidermis. Thus, the neurites wait for their targets. This sequence of events suggests that receptor formation may be induced by innervation of primordial cells within the epidermis. Mechanoreceptors are first formed between day 3 and 4, while electroreceptors are first formed on day 7. Electroreceptor multiplication is observed for the first time at an age of 25 days and correlates with the onset of the JAR. The somata of the anterior lateral line nerve ganglion project afferents out to peripheral electroreceptors and also send axons centrally into the ELL. The first electroreceptive axons invade the ELL by day 6, and presumably a rough somatotopic organization and segmentation within the ELL may arise as early as day 7. Axonal projections from the ELL to the torus develop after day 18.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗
PubMed1992

An internal current source yields immunity of electrosensory information processing to unusually strong jamming in electric fish.

The electric organ of a fish represents an internal current source, and the largely isopotential nature of the body interior warrants that the current associated with the fish's electric organ discharges (EODs) recruits all electroreceptors on the fish's body surface evenly. Currents associated with the EODs of a neighbor, however, will not penetrate all portions of the fish's body surface equally and will barely affect regions where the neighbor's current flows tangentially to the skin surface. The computational mechanisms of the jamming avoidance response (JAR) in Eigenmannia exploit the uneven effects of a neighbor's EOD current to calculate the correct frequency difference between the two interfering EOD signals even if the amplitude of a neighbor's signal surpasses that of the fish's own signal by orders of magnitude. The particular geometry of the fish's own EOD current thus yields some immunity against the potentially confusing effects of unusually strong interfering EOD currents of neighbors.

Animals↗
PubMed1991

Somatostatin-like immunoreactivity in the region of the prepacemaker nucleus in weakly electric knifefish, Eigenmannia: a quantitative analysis.

The diencephalic prepacemaker nucleus (PPn) is a bilateral cluster of neurons that controls frequency modulations of the otherwise very regular electric organ discharge cycle in weakly electric knifefish, Eigenmannia. Ultrastructural evidence had suggested that the action of excitatory and inhibitory synapses contacting PPn neurons is modulated by neuropeptides. In this investigation, we examined the distribution of somatostatin-like immunoreactive (S-IR) structures in the region of the PPn. In transverse sections, we found 5 bilateral S-IR structures in the region of the PPn: a 'dorsohorizontal stripe'; a 'lateral cell group'; a 'diagonal stripe'; a 'tubercular stripe'; and a 'hypothalamic stripe'. The dorsohorizontal stripe, consisting of S-IR fibers, terminals, and roughly 200 cell bodies unilaterally, stretches from the edge of the third ventricle at the thalamic dorsal-posterior nucleus and the central posterior nucleus approximately 400 microns laterally to the PPn. S-IR cell bodies show a distinct pattern of distribution within this stripe. Almost half of the somata are located within 50 microns of the ventricle. These ventricular cells are small and often densely clustered. Laterally, towards the PPn, the number of labelled cells decreases, whereas their size gradually increases. The lateral cell group consists of roughly 20 somata in the medial region of the subelectrosensorius nucleus. Fibers of the diagonal stripe travel from the hypothalamus dorsalis to the PPn. Fibers of the tubercular stripe originate from S-IR cell bodies in the medial zone of the periventricular nucleus of the posterior tuberculum and merge with the diagonal stripe. Fibers of the hypothalamic stripe connect the hypothalamus lateralis and the diagonal stripe. The density of immunolabelling in the hypothalamic stripe is significantly higher in mature than in immature females.

Animals↗
PubMed1991

The control of pacemaker modulations for social communication in the weakly electric fish Sternopygus.

Nearly sinusoidal electric organ discharges (EODs) of the weakly electric fish Sternopygus, occur at a regular rate within a range from 50 to 200 Hz and are commanded by a medullary pacemaker nucleus (Pn). During courtship and aggression, the rate of EODs is modulated as smooth EOD-frequency rises or brief EOD-interruptions (Hopkins 1974b). The present study examines the control of such modulations. Rises were elicited by L-glutamate stimulation of the diencephalic prepacemaker nucleus, the only previously known source of input to the Pn. We demonstrate an additional input to the Pn, the sublemniscal prepacemaker nucleus (SPPn). L-glutamate stimulation of this area caused EOD-interruptions. The Pn contains electrotonically coupled 'pacemaker cells' which generate the rhythm of the EODs, as well as 'relay cells' which transmit the command pulse to the spinal motor neurons that innervate the electric organ. Pacemaker cells recorded intracellularly during EOD-interruptions continued firing at their regular frequency but with slightly increased jitter. Relay cells, on the other hand, were strongly depolarized and fired spikelets at a greatly increased frequency during EOD-interruptions. Thus EOD-interruptions were caused by SPPn input to relay cells that caused their massive depolarization, blocking the normal input from pacemaker cells without greatly affecting pacemaker cell firing characteristics. Application to the Pn of an antagonist to NMDA-type glutamate receptors blocked EOD-frequency rises and EOD-interruptions. Antagonists to quisqualate/kainate receptor-types were ineffective.

Animal Communication↗
PubMed1991

The development of the Jamming Avoidance Response (JAR) in Eigenmannia: an innate behavior indeed.

In its Jamming Avoidance Response (JAR), the gymnotiform electric fish Eigenmannia shifts its electric organ discharge (EOD) frequency away from similar interfering frequencies. Continual behavioral measurements were carried out in 164 juvenile fish until a correct JAR emerged. Sixty-four of these fish were raised in complete isolation, the remainder in a community of their siblings. A correct JAR emerged in fish of 1.2-1.6 cm in body length, corresponding to a developmental age of 24-32 days. In 6 of 164 fish, the emergence of a correct JAR followed an interim appearance of an incorrect JAR, which involved frequency shifts in the direction opposite to those of a correct JAR. The fish raised in isolation developed the same forms of behavior and showed the same sequence in their appearance as did socially raised fish. This indicates that the JAR and its developmental schedule are innate. The appearance of an incorrect JAR suggests initial errors or incompleteness in the wiring of central nervous connections. A correct JAR ultimately emerged even if a stimulus regimen was offered that 'rewarded' frequency shifts in the direction opposite to those of a correct JAR. This indicates that the development of the JAR is immune to experimental alterations of sensory experience.

Animals↗
PubMed1991

The coding of signals in the electric communication of the gymnotiform fish Eigenmannia: from electroreceptors to neurons in the torus semicircularis of the midbrain.

In the context of aggression and courtship, Eigenmannia repeatedly interrupts its electric organ discharges (EODs) These interruptions contain low-frequency components as well as high-frequency transients and, therefore, stimulate ampullary and tuberous electroreceptors, respectively. Information provided by these two classes of receptors is relayed along separate pathways, via the electrosensory lateral line lobe (ELL) of the hindbrain, to the dorsal torus semicircularis (TSd) of the midbrain. Some neurons of the torus receive inputs from both types of receptors and some respond predominantly to EOD interruptions while being rather insensitive to other forms of signal modulations. This high selectivity appears to result from convergence and gating of inputs from individually less selective neurons.

Aggression↗
PubMed1991

Structure and function of neurons in the complex of the nucleus electrosensorius of the gymnotiform fish Eigenmannia: detection and processing of electric signals in social communication.

The complex of the diencephalic nucleus electrosensorius (nE) provides an interface between the electrosensory processing performed by the torus semicircularis and the control of specific behavioral responses. The rostral portion of the nE comprises two subdivisions that differ in the response properties and projection patterns of their neurons. First, the nEb, which contains neurons that are driven almost exclusively by beat patterns generated by the interference of electric organ discharges (EODs) of similar frequencies. Second, the area medial to the nEb, comprising the lateral pretectum (PT) and the nE-acusticolateralis region (nEar, 1 B-D), which contains neurons excited predominantly by EOD interruptions, signals associated with aggression and courtship. Neurons in the second area commonly receive convergent inputs originating from ampullary and tuberous electroreceptors, which respond to the low-frequency and high-frequency components of EOD interruptions, respectively. Projections of these neurons to hypothalamic areas linked to the pituitary may mediate modulations of a fish's endocrine state that are caused by exposure to EOD interruptions of its mate.

Aggression↗
PubMed1991

Recent advances in the study of electroreception.

Recent studies on electroreception in fish have focused on the structure and function of recurrent descending pathways, efference copy mechanisms, and multiple neuronal maps involved in the processing of sensory information. Studies on a neuronal oscillator have revealed that different neuronal inputs modulate the pattern of oscillations to produce different forms of behavioral output.

Animals↗
PubMed1991

Sensory control of behavior in electric fish.

The electrosensory system is ideally suited for the integration of behavioral and cellular approaches and, therefore, has led to the most detailed explanations of natural behaviors at the single-cell level. The electric sense shares basic principles in the coding of sensory information with more advanced sensory modalities and thus provides a convenient model system for studying neuronal mechanisms of information processing in general.

Animals↗
PubMed1990

Structural and functional organization of a diencephalic sensory-motor interface in the gymnotiform fish, Eigenmannia.

The diencephalic nucleus electrosensorius (nE) of gymnotiform fish comprises a series of finely tuned neuronal filters for control of the jamming avoidance response (JAR) and probably other electromotor tasks as well. The nE receives electrosensory input from the dorsal torus semicircularis (TSd) and octavolateral input from the ventral torus (TSv). The nE, in turn, projects to various hypothalamic and thalamic nuclei, including the prepacemaker nucleus (PPn), which can modulate the frequency of electric organ discharges (EODs) via its unique input to the medullary pacemaker nucleus. Four subdivisions of the nE can now be recognized: 1) The beat-related area (nEb)--a rostral cluster of tightly packed cells which receives TSd input and projects to the inferior lobe, anterior tuberal nucleus, anterior thalamic nucleus, central posterior thalamic nucleus, and PPn. The nEb contains neurons responsive to beat patterns caused by jamming stimuli. Stimulation of the nEb with L-glutamate, however, fails to induce any EOD-frequency shift. 2) The area causing EOD-frequency rises (nE increases)--a horizontal band of cells at the dorsal aspect of the caudal nE which receives TSd input and projects to the PPn and vicinity and to the cerebellum; nE increases stimulation induces slow EOD-frequency rises characteristic of the JAR. Responses of these cells to jamming stimuli are not yet known. 3) The area causing EOD-frequency falls (nE decreases)--a horizontal band of cells at the ventral aspect of the caudal nE which receives TSd input and projects only to the PPn and vicinity; nE decreases stimulation induces slow EOD-frequency falls characteristic of the JAR. The responses of these cells to jamming stimuli are not yet known. 4) The acousticolateral region (nEar)--a complex medial region of the nE which receives input predominantly from the ventral torus and projects to the inferior lobe, anterior tuberal nucleus, central posterior thalamic nucleus, PPn, and cerebellum; the sensory and motor properties of this region are not known in detail, although auditory and mechanosensory responses have been recorded here. Projections to the PPn and its vicinity suggest direct control of electromotor behaviors by the nE, whereas thalamic and hypothalamic projections may provide a substrate for electrosensory influences on neuroendocrine and motivational control centers. The optic tectum projects strongly to the pretectum and various other diencephalic nuclei in the vicinity of the nE, but it does not innervate the nE itself. Accordingly, ablation of the tectum does not affect the performance of the JAR.

Animals↗
PubMed1990

Electrosensory systems in fish.

A close integration of behavioral, neurophysiological, and neuroanatomical approaches has guided research on the neural basis of electrosensation and the generation of behaviors associated with this modality. By postulating neuronal implementations of specific computations in sensory information processing, behavioral studies have been crucial in focusing studies at the neuronal level onto behaviorally relevant structural and functional aspects. Physiological and anatomical studies have analyzed a) neural networks underlying the distributed processing of sensory information, b) the role of descending recurrent pathways and efference copy mechanisms for the filtering of incoming information, c) the significance of multiple topographic representations for sensory information processing, and d) the modulation of sensory and motor structures through various transmitters and receptor subtypes. Developmental studies have explored the significance of steroid hormones for the tuning of electroreceptors to the frequency of an endogenous neuronal oscillator which drives the electric current pulses necessary for their stimulation. Embryological studies have revealed that the development of mechanoreceptors and electroreceptors in the fish's skin is induced by the innervation of primary afferent nerve fibers which are specific with regard to their central connections as well as with regard to the type of receptor induced in the periphery.

Animals↗
PubMed1990

Different classes of glutamate receptors and GABA mediate distinct modulations of a neuronal oscillator, the medullary pacemaker of a gymnotiform electric fish.

Gymnotiform electric fish generate distinct communicatory signals by modulating the rate of their electric organ discharges (EODs). Each EOD is triggered by a command pulse from the medullary pacemaker nucleus (PN), which contains pacemaker cells and relay cells. The firing rate of this nucleus is modulated by inputs from the diencephalic prepacemaker nucleus (PPN). The NMDA receptor blocker APV and the kainate/quisqualate receptor blocker CNQX, administered to the PN, suppress different types of modulations, indicating that different classes of glutamate receptors mediate the generation of different modulations. A comparison of the 2 genera, Hypopomus and Eigenmannia, reveals that sustained modulations, such as smooth rises in the rate of pacemaker cell firing and the selective silencing of the relay cells (only observed in Hypopomus), are mediated by NMDA receptors, whereas the brief and rapid acceleration, called "chirp" or "decrement burst," is mediated by kainate/quisqualate receptors. Application of the GABA blocker bicuculline reveals that the 2 genera differ in the mechanism by which they slow the firing rate of their pacemaker. Whereas Hypopomus uses GABAergic inhibition to slow down and ultimately silence its pacemaker cells, Eigenmannia reduces tonic, APV-sensitive excitation originating from its PPN and lacks GABAergic inhibition in the PN.

2-Amino-5-phosphonovalerate↗
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↗