Signals and noise in the elasmobranch electrosensory system

Analyzing signal and noise for any sensory system requires an appreciation of the biological and physical milieu of the animal. Behavioral studies show that elasmobranchs use their electrosensory systems extensively for prey detection, but also for mate recognition and possibly for navigation. These biologically important signals are detected against a background of self-generated bioelectric fields. Noise-suppression mechanisms can be recognized at a number of different levels: behavior, receptor anatomy and physiology, and at the early stages of sensory processing. The peripheral filters and receptor characteristics provide a detector with permissive temporal properties but restrictive spatial characteristics. Biologically important signals probably cover the range from direct current to 10 Hz, whereas the bandwidth of the receptors is more like 0.1-10 Hz. This degree of alternating current coupling overcomes significant noise problems while still allowing the animal to detect external direct current signals by its own movement. Self-generated bioelectric fields modulated by breathing movement have similar temporal characteristics to important external signals and produce very strong modulation of electrosensory afferents. This sensory reafference is essentially similar, or common-mode, across all afferent fibers. The principal electrosensory neurons (ascending efferent neurons; AENs) of the dorsal octavolateralis nucleus show a greatly reduced response to common-mode signals. This suppression is mediated by the balanced excitatory and inhibitory components of their spatial receptive fields. The receptive field characteristics of AENs determine the information extracted from external stimuli for further central processing.

Adaptive mechanisms in the elasmobranch hindbrain

The suppression of self-generated electrosensory noise (reafference) and other predictable signals in the elasmobranch medulla is accomplished in part by an adaptive filter mechanism, which now appears to represent a more universal form of the modifiable efference copy mechanism discovered by Bell. It also exists in the gymnotid electrosensory lateral lobe and mechanosensory lateral line nucleus in other teleosts. In the skate dorsal nucleus, motor corollary discharge, proprioceptive and descending electrosensory signals all contribute in an independent and additive fashion to a cancellation input to the projection neurons that suppresses their response to reafference. The form of the cancellation signal is quite stable and apparently well-preserved between bouts of a particular behavior, but it can also be modified within minutes to match changes in the form of the reafference associated with that behavior. Motor corollary discharge, proprioceptive and electrosensory inputs are each relayed to the dorsal nucleus from granule cells of the vestibulolateral cerebellum. Direct evidence from intracellular studies and direct electrical stimulation of the parallel fiber projection support an adaptive filter model that places a principal site of the filter's plasticity at the synapses between parallel fibers and projection neurons.

The generation and subtraction of sensory expectations within cerebellum-like structures.

The generation of expectations about sensory input and the subtraction of such expectations from actual input appear to be important features of sensory processing. This paper describes the generation of sensory expectations within cerebellum-like structures of four distinct groups of fishes: Mormyridae; Rajidae; Scorpaenidae; and Apteronotidae. These structures consist of a sheet-like array of principal cells. Apical dendrites of the principal cells extend out into a molecular layer where they are contacted by parallel fibers. The basilar regions of the arrays receive primary afferent input from octavolateral endorgans, i.e., electroreceptors, mechanical lateral line neuromasts, or eighth nerve endorgans. The parallel fibers in the molecular layer convey various types of information, including corollary discharge signals associated with motor commands, sensory information from other modalities such as proprioception, and descending input from higher stages of the sensory modality that is processed by the structure. Associations between the signals conveyed by the parallel fibers and particular patterns of sensory input to the basal layers lead to the generation of a negative image of expected sensory input within the principal cell array. Addition of this negative image to actual sensory input results in the subtraction of expected from actual input, allowing the unexpected or novel input to stand out more clearly. Intracellular recording indicates that the negative image is probably generated by means of anti-Hebbian synaptic plasticity at the parallel fiber to principal cell synapse. The results are remarkably similar in the different fishes and may generalize to cerebellum-like structures in other sensory systems and taxa.

Distinct but overlapping populations of commissural and GABAergic neurons in the dorsal nucleus of the little skate, Raja erinacea.

In the little skate, Raja erinacea, the electrosensory primary afferents are responsive to electrical potentials created during the animal's own ventilation, while second-order electrosensory cells in the dorsal nucleus of the medulla suppress the responses to ventilatory potentials but retain their extreme sensitivity to important environmental electric signals. Previous electrophysiological studies indicate a role for a commissural pathway between the bilateral dorsal nuclei in ventilatory noise suppression. In the present study, retrograde tracers were used to label dorsal nucleus commissural cells. Large round or triangular and thin elongate commissural cells occur in the central zone of the dorsal nucleus where the primary afferent fibers terminate. Elongate commissural cells also occur in the peripheral zone which is the cell body area of the major efferents of the dorsal nucleus. Immunohistochemical studies indicate that stellate cells of the molecular layer and round or triangular cells of the central zone comprise the GABA-immunoreactive cell groups of the dorsal nucleus. A subpopulation of the round commissural cells in the central zone are GABA-immunoreactive and may be candidates for mediators of common-mode noise rejection in the dorsal nucleus of skates. The non-GABAergic commissural cells may mediate crossed inhibition through an inhibitory transmitter other than GABA or may supply crossed excitation to the dorsal nucleus.

A role for GABAergic inhibition in electrosensory processing and common mode rejection in the dorsal nucleus of the little skate, Raja erinacea.

The electrosensory primary afferents in elasmobranchs are responsive to electric potentials created by the animal's own ventilation, while the second-order neurons (AENs) which receive this afferent input in the medulla suppress responses to ventilatory potentials but retain their extreme sensitivity to electric signals in the environment. Ventilatory potentials are common mode signals in elasmobranchs and a common mode rejection mechanism is one way the AENs suppress ventilatory noise. By pressure injecting the GABA-A receptor antagonist SR95531 while extracellularly recording from AENs, we tested the hypothesis that the subtractive circuitry that selectively reduces common mode signals in AENs utilizes GABA, and that a GABAergic component of the dorsal nucleus commissural pathway mediates crossed inhibition of AENs. Local application of SR95531 increased the spontaneous activity and the responsiveness of AENs to electrosensory stimuli. AEN responses to a common mode stimulus were selectively increased compared to responses to a localized stimulus due to SR95531 application. Contralateral inhibition of AENs was blocked by SR95531, indicating that GABAergic commissural cells may inhibit AENs when the contralateral side of the body is stimulated, as with common mode stimulation. We conclude that GABAergic inhibition contributes significantly to the shaping of AEN responses including common mode rejection.

Motor corollary discharge activity and sensory responses related to ventilation in the skate vestibulolateral cerebellum: implications for electrosensory processing

The dorsal granular ridge (DGR) of the elasmobranch vestibulolateral cerebellum is the source of a parallel fiber projection to the electrosensory dorsal nucleus. We report that the DGR in Raja erinacea contains a large percentage of units with activity modulated by the animal's own ventilation. These include propriosensory and electrosensory units, responding to either ventilatory movements or the resulting electroreceptive reafference, and an additional population of units in which activity is phase-locked to the ventilatory motor commands even in animals paralyzed to block all ventilatory movements. A principal function of processing in the dorsal nucleus is the elimination of ventilatory noise in second-order electrosensory neurons. The existence of these ventilatory motor corollary discharge units, along with other DGR units responsive to ventilatory movements, suggests that the parallel fiber projection is involved in the noise cancellation mechanisms.

Hindbrain signal processing in the lateral line system of the dwarf scorpionfish Scopeana papillosus

Recordings were made from primary afferent fibres and secondary projection neurones (crest cells) in the mechanosensory lateral line system of the dwarf scorpionfish. Crest cells were identified by antidromic stimulation from the contralateral midbrain. Differences between primary afferent fibre and crest cell response characteristics are indicative of signal processing by the neuronal circuitry of the medial octavolateralis nucleus. There are a number of differences between primary afferent fibres and crest cells. Primary afferents have relatively high levels of spontaneous activity (mean close to 40 impulses s-1) and many of them are strongly modulated by ventilation. By contrast, crest cells have a much lower rate of spontaneous activity that is not obviously modulated by ventilation. Primary afferents show a simple tonic response to a maintained stimulus, whereas crest cells show a variety of temporal response properties, but in general show a phasic/tonic response to the same prolonged stimulus. Afferents are most sensitive to frequencies of stimulation around 100 Hz; in contrast, crest cells show a strong suppression of activity at this frequency. Crest cells are most responsive around 50 Hz. These afferent/secondary comparisons show similarities with those reported for allied electrosensory and auditory pathways.

The cerebellar dorsal granular ridge in an elasmobranch has proprioceptive and electroreceptive representations and projects homotopically to the medullary electrosensory nucleus.

1. Response properties of neurons in the dorsal granular ridge (DGR) of the little skate, Raja erinacea, were studied in decerebrate, curarized fish. Sensory responses included proprioceptive (426 of 952; 45%) and electroreceptive units (526 of 952; 55%). Electroreceptive units responded to weak electric fields with a higher threshold than lower-order units and had large ipsilateral receptive fields, whose exact boundaries were often unclear but contained smaller, identifiable best areas. Proprioceptive units responded to displacement of the ipsilateral fin and were either position- or movement-sensitive. 2. Both proprioceptive and electroreceptive units showed a progression of receptive fields from anterior to posterior body in the rostral to caudal direction along the length of DGR. Sensory maps in DGR projected homotopically to the electrosensory somatotopy in the dorsal nucleus. Peak evoked potentials and units responding to local DGR stimulation occurred only in areas of the dorsal nucleus with receptive fields located within the composite receptive field at the DGR stimulation site. 3. Single shocks to DGR produced a short spike train followed by a prolonged suppression period in the medullary dorsal nucleus. These results have implications for the role of the parallel fiber system in medullary electrosensory processing.

An adaptive filter that cancels self-induced noise in the electrosensory and lateral line mechanosensory systems of fish.

In lateral line and electrosensory systems of fish, the animal's own movements create unwanted stimulation that could interfere with the detection of biologically important signals. Here we report that an adaptive filter in the medullary nuclei of both senses suppresses self-stimulation. Second-order electrosensory neurons in an elasmobranch fish and mechanosensory neurons in a teleost fish learn to cancel the effects of stimuli that are presented coupled to the fish's movements. A model is proposed for how the adaptive filter is realized by the cerebellar-like circuits of the hindbrain nuclei in these senses.

Medullary electrosensory processing in the little skate. II. Suppression of self-generated electrosensory interference during respiration.

1. Previous studies have demonstrated that the resting activity of electrosensory ALLN fibers is modulated by the animal's own respiratory activity and that all fibers innervating a single ampullary cluster are modulated with the same amplitude and phase relationship to ventilation. We demonstrate that ALLN fibers in the skate are modulated in this common-mode manner bilaterally, regardless of receptor group, orientation, or position of the receptor pore on the body surface (Fig. 2). 2. Ascending efferent neurons (AENs), which project to the electrosensory midbrain from the DON, are modulated through a much smaller portion of their dynamic range. AENs give larger responses to an extrinsic local electric field than to the respiratory driving, indicating that a mechanism exists for suppressing ventilatory electrosensory reafference. 3. In paralyzed animals no modulation of resting activity or of responses of extrinsic electric fields could be observed with respect to the animal's respiratory motor commands in the absence of electrosensory reafference. 4. Cells of the dorsal granular ridge (DGR) project to medullary AENs via the DON molecular layer. A majority of proprioceptive DGR neurons are modulated by ventilatory activity, however, in a given fish the modulation is not in the same phase relationship to ventilation among DGR units. 5. The modulation of AENs during respiration was increased following transection of the contralateral ALLN (Fig. 9). Resting activity and responses to excitatory stimuli were inhibited by simultaneous stimulation of the transected contralateral ALLN indicating that a common-mode rejection mechanism is mediated via the commissural interconnections of the DONs.

Elasmobranch vision: multimodal integration in the brain.

Multimodal sensory areas that include vision have been identified physiologically in two separate pallial areas in the telencephalon and in the tectum of the mesencephalon. Multisensory integration occurs in the medial pallium of the little skate, Raja erinacea, and a primitive squalomorph shark, Squalus acanthias, whereas in the advanced galeomorph shark, Ginglymostoma cirratum, a major multimodal area is in the dorsal pallium pars centralis. Pars centralis has undergone extensive hypertrophy in the evolution of advanced batoids and galeomorph sharks. More complete studies are required on individual species to assess the possibility that there has been an evolutionary shift in major sensory processing areas from medial to dorsal pallium among the elasmobranchs. Most retinofugal fibers in elasmobranchs project spatiotopically to the tectum, the central zone of which is an area of multimodal integration. The spatiotopic tectal map of the electrosense in the little skate includes only that part of the electrosensory field that is within the visual field, and individual points on the tectum represent the same spatial location in each sense. In both maps the region of space near the horizon is greatly overrepresented. For vision this corresponds to a band of increased retinal ganglion cell density, and for both senses the overrepresentation may be related to the importance of this region of space in the skate's natural orienting. Spatial congruence of visual and electrosensory maps should ensure that individual tectal cells integrate multimodal information in a space-specific fashion.

Afferent and efferent connections of the vestibulolateral cerebellum of the little skate, Raja erinacea.

Horseradish peroxidase and cobaltous lysine tracers are used to determine the afferent and efferent projections of the vestibulolateral cerebellum (VLL) in the little skate, Raja erinacea. The skate VLL has separate divisions, pars medialis and pars lateralis, associated with vestibular and lateralis modalities, respectively. The pars medialis has a typical cerebellar structure with molecular and Purkinje cell layers and granular areas. In addition to known inputs from eighth nerve vestibular fibers and limited mechanosensory lateralis afferents, pars medialis afferents are from the ventral part of the descending octaval nucleus, the lateral funicular nucleus and nucleus of the medial longitudinal fasciculus. The pars lateralis and rostral anterior octaval nucleus may be additional afferent sources. Pars medialis efferents project to ventral descending and anterior octaval nuclei, as mossy fibers to the cerebellar corpus and as parallel fibers in the ventrolateral extreme of the molecular layer in the medial octavolateralis nucleus. The pars lateralis comprises granule and Golgi cells and is subdivided into a dorsal granular ridge (DGR) and lateral granular area (LG) that are the sources of parallel fibers in the molecular layers of the dorsal (electrosensory) and medial (mechanosensory) octavolateralis nuclei. Local injections of tracer reveal a systematic topography of pars lateralis parallel fiber projections and a mossy fiber projection to the corpus. Both DGR and LG receive direct spinal input but afferent sources to DGR and LG are otherwise distinct. While LG is known to receive mechanosensory lateralis afferents and limited eighth nerve fibers, DGR receives no direct cranial nerve input. Additional afferents to LG are predominantly from contralateral LG and the anterior octaval and lateral funicular nuclei. Additional DGR afferents are from three medullary nuclei beneath the cerebellar peduncle, nuclei F and K and paralemniscal nucleus, which also projects directly to the dorsal nucleus. Distinct inputs to DGR and LG suggest different contributions of VLL to medullary processing in electro- and mechanoreception.

End buds: non-ampullary electroreceptors in adult lampreys.

Shared anatomical and physiological characters indicate that the low-frequency sensitive electrosensory system of lampreys is homologous with those of non-teleost fishes and amphibians. However, the ampullary electroreceptor organs which characterize all of these gnathostomes are not found in lampreys. Experimental anatomical and physiological studies reported here demonstrate that the epidermal end buds are the electroreceptors of adult lampreys. End buds, consisting of both sensory and supporting cells, are goblet-shaped with the top (25-60 microns diameter) at the epidermal surface and the stem directed toward the dermis (Fig. 1A). Short lines or clusters of 2-8 end buds (Fig. 1B) are distributed over both trunk and head. Injections of horseradish peroxidase (HRP) into vitally-stained end buds labeled anterior lateral line afferents terminating in the ipsilateral dorsal nucleus (Fig. 2A) - the primary electrosensory nucleus of the lamprey medulla. Conversely, after HRP injection into the dorsal nucleus HRP-filled fibers and terminals were present on ipsilateral end buds (Fig. 2B). End buds are usually not visible without staining. However, in adult sea lampreys the presence of end buds was histologically confirmed in skin patches containing the receptive fields of electroreceptor fibers recorded in the anterior lateral line nerve. Additionally, in the rare instance of two silver lampreys in which end buds were visible without staining, electrosensory activity indistinguishable from that of the primary electroreceptor afferents was recorded from the end bud surface (Figs. 3, 4). End buds were initially characterized as chemoreceptors (Johnston 1902) but were later correctly advanced as lateralis receptors based on the presence of presynaptic dense bodies in the receptor cells (Whitear and Lane 1981).(ABSTRACT TRUNCATED AT 250 WORDS)

Segregation of electroreceptive and mechanoreceptive lateral line afferents in the hindbrain of chondrostean fishes.

The anterior lateral line nerve (ALLN) in the chondrostean fishes (sturgeon and paddlefishes) consists of both fibers innervating ampullary electroreceptors and fibers innervating the mechanoreceptive neuromasts of the cephalic lateral line system. The fibers of the posterior lateral line nerve (PLLN) innervate only mechanoreceptive neuromasts on the body trunk. The ALLN enters the medulla via dorsal and ventral roots; the dorsal root projects to the dorsal octavolateralis nucleus (DON), whereas the ventral root and the PLLN project principally to the medial octavolateralis nucleus (MON). Previous studies in elasmobranchs have demonstrated that fibers of the dorsal root of the ALLN convey electrosensory information, and fibers of the ventral root are concerned with mechanoreceptive information. Electrophysiological and neuroanatomical methods are employed in this study in order to determine if there exists a similar segregation of electroreceptive and mechanoreceptive lateral line afferents within the chondrostean medulla. In specimens of shovelnose, Scaphirhynchus platorynchus, and Atlantic sturgeon, Acipenser oxyrhynchus, and paddlefish, Polyodon spathula, evoked potentials recorded from the hindbrain and elicited by electric fields reached maximum amplitude within the DON and decreased in amplitude through the cerebellar crest. Evoked potentials elicited by stimulation of the posterior lateral line nerve achieved maximum amplitude within the MON. Single and multiple unit recordings revealed that units within the DON responded only to electric field stimulation, whereas units recorded in the MON responded only to mechanical stimulation. Horseradish peroxidase implanted beneath isolated patches of ampullae in Polyodon revealed fibers innervating electroreceptors projecting to the DON via the dorsal root of the ALLN. These results demonstrate a segregation of electroreceptive and mechanoreceptive lateral line afferent fibers in the chondrostean hindbrain, similar to that seen in elasmobranchs. This supports the contention that the electrosensory systems of elasmobranchs and chondrosteans are homologous, and are derived from the common ancestor of elasmobranch and actinopterygian fishes.

Somatotopy within the medullary electrosensory nucleus of the little skate, Raja erinacea.

The dorsal octavolateral nucleus is the primary electrosensory nucleus in the elasmobranch medulla. We have studied the topographic organization of electrosensory afferent projections within the dorsal nucleus of the little skate, Raja erinacea, by anatomical (HRP) and physiological experiments. The electrosensory organs (ampullae of Lorenzini) in skates are located in four groups on each side of the body, and each group is innervated by a separate ramus of the anterior lateral line nerve (ALLN). Transganglionic transport of HRP in individual rami demonstrated that electroreceptor afferents in each ramus project to a separate, nonoverlapping division of the central zone of the ipsilateral dorsal nucleus. These divisions, which are distinct areas separated by compact cell plates, are somatopically arranged. The volume of each division of the dorsal nucleus that is related to a single ramus is proportional to the number of ampullae innervated by the ramus, but not to the body surface area on which the receptors are distributed. Nearly one-half of the nucleus is devoted to electrosensory inputs from the buccal and superficial ophthalmic ampullae concentrated in a small area on the ventral surface of the head rostral to the mouth. Multiple and single unit recordings demonstrated that adjacent cells in the nucleus have similar receptive fields on the body surface and revealed a detailed point-to-point somatotopy within the nucleus. With threshold stimuli most single units have ipsilateral receptive fields made up by excitatory inputs from 2-5 ampullary organs. The somatotopy within the mechanosensory medial nucleus, also revealed by the HRP fills of individual ALLN rami, appears less rigid than that in the dorsal nucleus, as extensive overlap is present in the terminal fields of separate ALLN rami.

An electrosensory area in the telencephalon of the little skate, Raja erinacea.

On the basis of evoked potential and multiple unit responses we identified a pallial electrosensory area that extends throughout the central one-third of the skate telencephalon. This electrosensory area coincides in its mediolateral and rostrocaudal extent with an area of visual responsiveness. Throughout the area peak visual activity is 250-500 micrometers superficial to the maximum electrosensory responses. However, both electrosensory and visual areas appear to be located within the same pallial cell group. The depth and proximity of this pallial area to the lateral ventricle and medial forebrain bundle suggest that it is a subdivision of the medial pallium. Injection of HRP into the area from a glass microelectrode following recordings revealed retrogradely labeled cells in 3 separate diencephalic nuclei, the largest of which, the lateral posterior nucleus, also is responsive to electrosensory stimuli.