Modeling of time disparity detection by the Hodgkin-Huxley equations

Phase-sensitive neurons in the electrosensory lateral line lobe in the electrosensory pathway of the wave-type electric fish, Gymnarchus niloticus, are specialized for sensing the time disparity between sensory inputs at different parts of the body surface that is necessary for an electrical behavior, jamming avoidance response. These neurons are sensitive to time disparity in the microsecond range between synaptic inputs that represent occurrence times of electrosensory signals at different areas on the body surface. We showed that an ideal Hodgkin-Huxley equation may serve as a time disparity detector that fits physiological precision, and the precision for the time disparity detection is largely regulated by the maximal g(K) conductance in the Hodgkin-Huxley equations.     

The jamming avoidance response ofEigenmannia: properties of a diencephalic link between sensory processing and motor output

Summary Brain regions participating in the control ofEigenmannia's electric organ discharge frequency were localized by electrical microstimulation and anatomically identified by means of horseradish peroxidase deposition. A diencephalic region was found which, when stimulated, caused electric organ discharge (EOD) frequency increases of similar magnitude and time course as the frequency increases seen during the jamming avoidance response. Single unit recordings from this region revealed one cell type which preferentially responded to stimuli that cause the acceleration phase of the jamming avoidance response (electric organ discharge frequency increase). A second cell type responded preferentially to stimuli which cause EOD frequency decrease, and both cell types were tuned to stimuli which evoked maximal jamming avoidance behaviors.The results of the horseradish peroxidase experiments showed that the recording and stimulation sites correspond to the previously described nucleus electrosensorius. Our results confirm the earlier finding that this nucleus receives output from the torus semicircularis and we also found that the N. electrosensorius projects to the mesencephalic prepacemaker nucleus. The prepacemaker projects to the medullary pacemaker nucleus which generates the commands that evoke electric organ discharges.The anatomical and physiological results described here establish this diencephalic region as a link between the major sensory processing region for the jamming avoidance response, the torus semicircularis, and a mesencephalic pre-motor region, the prepacemaker nucleus.Abbreviations AM amplitude modulation - DF Delta F - ELLL electrosensory lateral line lobe - EOD electric organ discharge - JAR jamming avoidance response - NE nucleus electrosensorius - PPN prepacemaker nucleus - PN pacemaker nucleus     

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 prepacemaker nucleus can be recruited to raise the electric organ discharge frequency above the resting level. Another normally active input, from the sublemniscal prepacemaker 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 prepacemaker 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 prepacemaker do not affect performance of the jamming avoidance response. Thus, in Apteronotus, the sublemniscal prepacemaker alone controls the change of the electric organ discharge frequency during the jamming avoidance response.     

Walter Heiligenberg: the jamming avoidance response and beyond

Walter Heiligenberg (1938–1994) was an exceptionally gifted behavioral physiologist who made enormous contributions to the analysis of behavior and to our understanding of how the brain initiates and controls species-typical behavioral patterns. He was distinguished by his rigorous analytical approach used in both behavioral studies and neuroethological investigations. Among his most significant contributions to neuroethology are a detailed analysis of the computational rules governing the jamming avoidance response in weakly electric fish and the elucidation of the principal neural pathway involved in neural control of this behavior. Based on his work, the jamming avoidance response is perhaps the best-understood vertebrate behavior pattern in terms of the underlying neural substrate. In addition to this pioneering work, Heiligenberg stimulated research in a significant number of other areas of ethology and neuroethology, including: the quantitative assessment of aggressivity in cichlid fish; the ethological analysis of the stimulus–response relationship in the chirping behavior of crickets; the exploration of the neural and endocrine basis of communicatory behavior in weakly electric fish; the study of cellular mechanisms of neuronal plasticity in the adult fish brain; and the phylogenetic analysis of electric fishes using a combination of morphology, electrophysiology, and mitochondrial sequence data.T. H. Bullock: deceased 2005     

Effects of global electrosensory signals on motion processing in the midbrain of <Emphasis Type="Italic">Eigenmannia</Emphasis>

Wave-type weakly electric fish such as Eigenmannia produce continuous sinusoidal electric fields. When conspecifics are in close proximity, interaction of these electric fields can produce deficits in electrosensory function. We examined a neural correlate of such jamming at the level of the midbrain. Previous results indicate that neurons in the dorsal layers of the torus semicircularis can (1) respond to jamming signals, (2) respond to moving electrosensory stimuli, and (3) receive convergent information from the four sensory maps of the electrosensory lateral line lobe (ELL). In this study we recorded the intracellular responses of both tuberous and ampullary neurons to moving objects. Robust Gaussian-shaped or sinusoidal responses with half-height durations between 55 ms and 581 ms were seen in both modalities. The addition of ongoing global signals with temporal-frequencies of 5 Hz attenuated the responses to the moving object by 5 dB or more. In contrast, the responses to the moving object were not attenuated by the addition of signals with temporal frequencies of 20 Hz or greater. This occurred in both the ampullary and tuberous systems, despite the fact that the ampullary afferents to the torus originate in a single ELL map whereas the tuberous afferents emerge from three maps.     

Independently evolved jamming avoidance responses employ identical computational algorithms: a behavioral study of the African electric fish,Gymnarchus niloticus

An African electric fish, Gymnarchus, and a South American electric fish, Eigenmannia, are believed to have evolved their electrosensory systems independently. Both fishes, nevertheless, gradually shift the frequency of electric organ discharge away when they encounter a neighbor of a similar discharge frequency. Computational algorithms employed by Gymnarchus for this jamming avoidance response have been identified in this study for comparison with those of extensively studied Eigenmannia.

1. Gymnarchus determines whether it should raise or lower its discharge frequency based solely upon the signal mixture of its own reafferent and the exafferent signal from a neighbor, and does not internally refer to the pacemaker command signal which drives its own discharge.
2. The signal mixture is analyzed in terms of the time courses of amplitude modulation and phase modulation at each area of the body surface.
3. Phase of the signal mixture at each area is compared with that of another area for the detection of phase modulation.
4. Unambiguous information necessary for the jamming avoidance response is extracted by integrating information from all body areas each of which yields ambiguous information.
5. These computational features are identical to those of Eigenmannia, suggesting that the neural circuit for jamming avoidance responses may have evolved from preexisting mechanisms for electrolocation in both fishes.

     

Single unit activity in the mesencephalon of Sternarchus

Action potentials evoked in a phase-locked 1 : 1 relationship by natural electric organ discharges (EOD) were recorded extracellularly and intracellularly from single mesencephalic magnocellular nucleus units in the high frequency electric fish Sternarchus albifrons (Gymnotidae). This activity has been shown to be the result of an extrinsic feedback of the electrosensory system and is probably important for the socalled jamming avoidance response triggered artificial electric pulses when delivered into the water in a 1 : 1 relationship at intensities higher than the EOD. In the same way, artificial pulses of frequency near EOD could either drive or, due to beats, greatly disturb the regular firing of the units. More insight into the neural mechanism was yielded by single EOD-triggered shocks provoking a failure in firing of certain action potentials of the series and causing long-lasting (10-20 ms) accelerations and decelerations of the regular EOD-evoked firing (transient disturbance). Intracellular stimulations show similar effects. The biological significance of this neural mechanism for the fish's electroperception and JAR is discussed.     

Spatiotemporal burst coding for extracting features of spatiotemporally varying stimuli

Encoding features of spatiotemporally varying stimuli is quite important for understanding the neural mechanisms of various sensory coding. Temporal coding can encode features of time-varying stimulus, and population coding with temporal coding is adequate for encoding spatiotemporal correlation of stimulus features into spatiotemporal activity of neurons. However, little is known about how spatiotemporal features of stimulus are encoded by spatiotemporal property of neural activity. To address this issue, we propose here a population coding with burst spikes, called here spatiotemporal burst (STB) coding. In STB coding, the temporal variation of stimuli is encoded by the precise onset timing of burst spike, and the spatiotemporal correlation of stimuli is emphasized by one specific aspect of burst firing, or spike packet followed by silent interval. To show concretely the role of STB coding, we study the electrosensory system of a weakly electric fish. Weakly electric fish must perceive the information about an object nearby by analyzing spatiotemporal modulations of electric field around it. On the basis of well-characterized circuitry, we constructed a neural network model of the electrosensory system. Here we show that STB coding encodes well the information of object distance and size by extracting the spatiotemporal correlation of the distorted electric field. The burst activity of electrosensory neurons is also affected by feedback signals through synaptic plasticity. We show that the control of burst activity caused by the synaptic plasticity leads to extracting the stimulus features depending on the stimulus context. Our results suggest that sensory systems use burst spikes as a unit of sensory coding in order to extract spatiotemporal features of stimuli from spatially distributed stimuli.     

Neural correlates of novelty detection in pulse-type weakly electric fish

Evoked potentials (EPs) and single unit recordings from various electrosensory-processing regions of several pulse-type gymnotiform species were made to investigate neural activity patterns that could be associated with novelty detection. Whereas the electrosensory afferents and cells in the ELL exhibited only minor changes in response size as stimuli were presented less frequently (novel stimuli), most units studied in the torus semicircularis (TS) showed very strong, increased responsiveness to stimuli presented less frequently relative to stimuli presented persistently (at every EOD event. The responses of the TS were graded with respect to stimulus frequency. The discrimination between novel and persistent stimuli by the TS occurred with stimuli presented transversely or longitudinally with respect to the fish's long axis, and regardless of the timing of the stimulus with respect to the fish's pacemaker-related signal (PS). When electrosensory novelties were presented persistently the responses of the TS rapidly habituated. This may indicate that activity in this region of the TS is novelty related. This novelty-related activity in the TS can be correlated with certain aspects of the fish's behavior, i.e., EOD interval length during a behavioral novelty response. However, TS activity may continue to indicate the occurrence of electrosensory novelties after the behavior has habituated. It is suggested that the novelty-related activity of the TS of these fish is necessary, but not sufficient, for the production of electrosensory novelty-induced behavioral responses. Lesions of the region of the TS containing the rapidly-habituating neurons abolished the electrosensory novelty response, but not that resulting from visual and auditory stimulation.     

Design principles of sensory processing in cerebellum-like structures

Cerebellum-like structures are compared for two sensory systems: electrosensory and auditory. The electrosensory lateral line lobe of mormyrid electric fish is reviewed and the neural representation of electrosensory objects in this structure is modeled and discussed. The dorsal cochlear nucleus in the auditory brainstem of mammals is reviewed and new data are presented that characterize the responses of neurons in this structure in the mouse. Similarities between the electrosensory and auditory cerebellum-like structures are shown, in particular adaptive processes that may reduce responses to predictable stimuli. We suggest that the differences in the types of sensory objects may drive the differences in the anatomical and physiological characteristics of these two cerebellum-like structures.     

The African wave-type electric fish,Gymnarchus niloticus,lacks corollary discharge mechanisms for electrosensory gating

Gymnarchus niloticus, a wave-type African electric fish, performs its jamming avoidance response by relying solely upon afferent signals and does not use corollary discharges from the pacemaker nucleus in the medulla which generates the rhythmicity of electric organ discharges. This is in sharp contrast to the mode of sensory processing found in closely related African pulse-type electric fishes where afferent signals are gated by corollary discharges from the pacemaker for the distinction of exafferent and reafferent stimuli. Does Gymnarchus still possess a corollary discharge mechanism for other behavioral tasks but does not use it for the jamming avoidance response? In this study, I recorded from and labeled medullary neuronal structures that either generate or convey the pacemaker signal for electric organ discharges to examine whether this information is also sent directly to any sensory areas. The pacemaker nucleus was identified as the site of generation of the pacemaking signal. The pacemaker neurons project exclusively to the lateral relay nucleus which, in turn projects exclusively to the medial relay nucleus. Neurons in the medial relay nucleus send unbranched axons to the spinal electromotoneurons. These neurons are entirely devoted to drive the electric organ discharges, and no axon collaterals from these neurons were found to project to any sensory areas. This indicates that Gymnarchus does not possess the neuronal hardware for a corollary discharge mechanism.     

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)     

Temporal Hyperacuity in the Gymnotiform Electric Fish, Eigenmannia

SYNOPSIS. The gymnotiform electric fish, Eigenmannia, exhibitsextraordinary sensitivity to small timing differences betweensensory signals. The jamming avoidance response, gradual frequencyshifts of the electric organ discharges, requires the detectionof temporal disparities between sensory signals impinging upondifferent electroreceptors. This behavior occurs reliably evenwith temporal disparities being smaller than one microsecond.Since individual sensory receptors are not capable of encodingsuch minute timing with certainty, the high behavioral sensitivitymust, therefore, emerge from signal processing within the centralnervous system. Individual neurons, at the top of a well definedneuronal hierarchy have been found to be sensitive to temporaldisparities in the range of 1 microsecond. The response propertiesof these neurons as well as behavioral results suggest thatspatial convergence of sensory information plays a major rolein the emergence of this temporal hyperacuity.     

‘Ancestral’ neural mechanisms of electrolocation suggest a substrate for the evolution of the jamming avoidance response

Summary The genusSternopygus, believed to reflect ancestral traits of gymnotiform electric fish, is closely related to the more modern genusEigenmannia (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 inEigenmannia, we found thatSternopygus 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 inEigenmannia, 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 inSternopygus. 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.Abbreviations AM amplitude modulation - Df frequency difference - EOD electric organ discharge - JAR jamming avoidance response     

Behavioral guides for sensory neurophysiology

The study of natural behavior is important for understanding the coding schemes of sensory systems. The jamming avoidance response of the weakly electric fish Eigenmannia is an excellent example of a bottom–up approach, in which behavioral analyses guided neurophysiological studies. These studies started from the electroreceptive sense organs to the motor output consisting of pacemaker neurons. Going in the opposite direction, from the central nervous system to lower centers, is the characteristic of the top–down approach. Although this approach is perhaps more difficult than the bottom–up approach, it was successfully employed in the neuroethological analysis of sound localization in the barn owl. In the latter studies, high-order neurons selective for complex natural stimuli led to the discovery of neural pathways and networks responsible for the genesis of the stimulus selectivity. Comparison of Eigenmannia and barn owls, and their neural systems, has revealed similarities in network designs, such as parallel pathways and their convergence to produce stimulus selectivity necessary for detection of natural stimuli.     

Responses of neurons in the electrosensory lateral line lobe of the weakly electric fish <Emphasis Type="Italic">Gnathonemus petersii</Emphasis> to simple and complex electrosensory stimuli

Mormyrid fish use active electrolocation to detect and analyze objects. The electrosensory lateral line lobe in the brain receives input from electroreceptors and an efference copy of the command to discharge the electric organ. In curarized fish, we recorded extracellularly from neurons of the electrosensory lateral line lobe while stimulating in the periphery with either a local point stimulus or with a more natural whole-body stimulus. Two classes of neurons were found: (1) three types of E-cells, which were excited by a point stimulus; and (2) two types of I-cells, which were inhibited by point stimulus and responded with excitation to the electric organ corollary discharge. While all neurons responded to a point stimulus, only one out of two types of I-units and two of the three types of E-units changed their firing behavior to a whole-body stimulus or when an object was present. In most units, the responses to whole-body stimuli and to point stimuli differed substantially. Many electrosensory lateral line lobe units showed neural plasticity after prolonged sensory stimulation. However, plastic effects during whole body stimulation were often unlike those occurring during point stimuli, suggesting that under natural conditions electrosensory lateral line lobe network effects play an important role in shaping neural plasticity.     

Encoding and processing biologically relevant temporal information in electrosensory systems

Wave-type weakly electric fish are specialists in time-domain processing: behaviors in these animals are often tightly correlated with the temporal structure of electrosensory signals. Behavioral responses in these fish can be dependent on differences in the temporal structure of electrosensory signals alone. This feature has facilitated the study of temporal codes and processing in central nervous system circuits of these animals. The temporal encoding and mechanisms used to transform temporal codes in the brain have been identified and characterized in several species, including South American gymnotid species and in the African mormyrid genus Gymnarchus. These distantly related groups use similar strategies for neural computations of information on the order of microseconds, milliseconds, and seconds. Here, we describe a suite of mechanisms for behaviorally relevant computations of temporal information that have been elucidated in these systems. These results show the critical role that behavioral experiments continue to have in the study of the neural control of behavior and its evolution.     

Omnidirectional sensory and motor volumes in electric fish

Active sensing organisms, such as bats, dolphins, and weakly electric fish, generate a 3-D space for active sensation by emitting self-generated energy into the environment. For a weakly electric fish, we demonstrate that the electrosensory space for prey detection has an unusual, omnidirectional shape. We compare this sensory volume with the animal's motor volume—the volume swept out by the body over selected time intervals and over the time it takes to come to a stop from typical hunting velocities. We find that the motor volume has a similar omnidirectional shape, which can be attributed to the fish's backward-swimming capabilities and body dynamics. We assessed the electrosensory space for prey detection by analyzing simulated changes in spiking activity of primary electrosensory afferents during empirically measured and synthetic prey capture trials. The animal's motor volume was reconstructed from video recordings of body motion during prey capture behavior. Our results suggest that in weakly electric fish, there is a close connection between the shape of the sensory and motor volumes. We consider three general spatial relationships between 3-D sensory and motor volumes in active and passive-sensing animals, and we examine hypotheses about these relationships in the context of the volumes we quantify for weakly electric fish. We propose that the ratio of the sensory volume to the motor volume provides insight into behavioral control strategies across all animals.     

Developmental origin of shark electrosensory organs

Vertebrates have evolved electrosensory receptors that detect electrical stimuli on the surface of the skin and transmit them somatotopically to the brain. In chondrichthyans, the electrosensory system is composed of a cephalic network of ampullary organs, known as the ampullae of Lorenzini, that can detect extremely weak electric fields during hunting and navigation. Each ampullary organ consists of a gel-filled epidermal pit containing sensory hair cells, and synaptic connections with primary afferent neurons at the base of the pit that facilitate detection of voltage gradients over large regions of the body. The developmental origin of electroreceptors and the mechanisms that determine their spatial arrangement in the vertebrate head are not well understood. We have analyzed electroreceptor development in the lesser spotted catshark (Scyliorhinus canicula) and show that Sox8 and HNK1, two markers of the neural crest lineage, selectively mark sensory cells in ampullary organs. This represents the first evidence that the neural crest gives rise to electrosensory cells. We also show that pathfinding by cephalic mechanosensory and electrosensory axons follows the expression pattern of EphA4, a well-known guidance cue for axons and neural crest cells in osteichthyans. Expression of EphrinB2, which encodes a ligand for EphA4, marks the positions at which ampullary placodes are initiated in the epidermis, and EphA4 is expressed in surrounding mesenchyme. These results suggest that Eph-Ephrin signaling may establish an early molecular map for neural crest migration, axon guidance and placodal morphogenesis during development of the shark electrosensory system.     

From sparks to spikes: information processing in the electrosensory systems of fish

Recent work on electrosensory systems in fish has combined traditional neuroethological approaches with quantitative methods for characterizing neural coding. These studies have shed light on general issues in sensory processing, including how peripheral sensory receptors encode external stimuli and how these representations are transformed at subsequent stages of processing.