Bi-sensory, striped representations: comparative insights from owl and platypus.

Bi-sensory striped arrays are described in owl and platypus that share some similarities with the other variant of bi-sensory striped array found in primate and carnivore striate cortex: ocular dominance columns. Like ocular dominance columns, the owl and platypus striped systems each involve two different topographic arrays that are cut into parallel stripes, and interdigitated, so that higher-order neurons can integrate across both arrays. Unlike ocular dominance stripes, which have a separate array for each eye, the striped array in the middle third of the owl tectum has a separate array for each cerebral hemisphere. Binocular neurons send outputs from both hemispheres to the striped array where they are segregated into parallel stripes according to hemisphere of origin. In platypus primary somatosensory cortex (S1), the two arrays of interdigitated stripes are derived from separate sensory systems in the bill, 40,000 electroreceptors and 60,000 mechanoreceptors. The stripes in platypus S1 cortex produce bimodal electrosensory-mechanosensory neurons with specificity for the time-of-arrival difference between the two systems. This "thunder-and-lightning" system would allow the platypus to estimate the distance of the prey using time disparities generated at the bill between the earlier electrical wave and the later mechanical wave caused by the motion of benthic prey. The functional significance of parallel, striped arrays is not clear, even for the highly-studied ocular dominance system, but a general strategy is proposed here that is based on the detection of temporal disparities between the two arrays that can be used to estimate distance.     

Passive electroreception in aquatic mammals

Passive electroreception is a sensory modality in many aquatic vertebrates, predominantly fishes. Using passive electroreception, the animal can detect and analyze electric fields in its environment. Most electric fields in the environment are of biogenic origin, often produced by prey items. These electric fields can be relatively strong and can be a highly valuable source of information for a predator, as underlined by the fact that electroreception has evolved multiple times independently. The only mammals that possess electroreception are the platypus (Ornithorhynchus anatinus) and the echidnas (Tachyglossidae) from the monotreme order, and, recently discovered, the Guiana dolphin (Sotalia guianensis) from the cetacean order. Here we review the morphology, function and origin of the electroreceptors in the two aquatic species, the platypus and the Guiana dolphin. The morphology shows certain similarities, also similar to ampullary electroreceptors in fishes, that provide cues for the search for electroreceptors in more vertebrate and invertebrate species. The function of these organs appears to be very similar. Both species search for prey animals in low-visibility conditions or while digging in the substrate, and sensory thresholds are within one order of magnitude. The electroreceptors in both species are innervated by the trigeminal nerve. The origin of the accessory structures, however, is completely different; electroreceptors in the platypus have developed from skin glands, in the Guiana dolphin, from the vibrissal system.     

A hormone-sensitive communication system in an electric fish

The electric communication system includes both special muscle-derived cells or electrocytes that produce species-typical electric signals, or electric organ discharges (EODs), and specialized sensory receptors, or electroreceptors, that encode the electric fields set up by EODs. Steroid hormones can influence the characteristic properties of both EODs and electroreceptors. Steroids appear to directly effect the anatomy and physiology of the electrocytes that generate an EOD. In contrast, the steroid effect on electroreceptors may be predominantly via an indirect mechanism whereby changes in the spectral characteristics of the EOD appear to induce changes in the spectral sensitivity of electroreceptors. Continued studies of electrosensory and electromotor systems will offer insights into the cellular bases for the development and evolution of steroid-sensitive pathways in the vertebrate nervous system.     

Tactile neural mechanisms in monotremes

Monotremes, perhaps more than any other order of mammals, display an enormous behavioural reliance upon the tactile senses. In the platypus, Ornithorhynchus anatinus, this is manifest most strikingly in the special importance of the bill as a peripheral sensory organ, an importance confirmed by electrophysiological mapping that reveals a vast area of the cerebral cortex allocated to the processing of tactile inputs from the bill. Although behavioural evidence in the echidna, Tachyglossus aculeatus, suggests a similar prominence for tactile inputs from the snout, there is also a great reliance upon the distal limbs for digging and burrowing activity, pointing to the importance of tactile information from these regions for the echidna. In recent studies, we have investigated the peripheral tactile neural mechanisms in the forepaw of the echidna to establish the extent of correspondence or divergence that has emerged over the widely different evolutionary paths taken by monotreme and placental mammals. Electrophysiological recordings were made from single tactile sensory nerve fibres isolated in fine strands of the median or ulnar nerves of the forearm. Controlled tactile stimuli applied to the forepaw glabrous skin permitted an initial classification of tactile sensory fibres into two broad divisions, according to their responses to static skin displacement. One displayed slowly adapting (SA) response properties, while the other showed a selective sensitivity to the dynamic components of the skin displacement. These purely dynamically-sensitive tactile fibres could be subdivided according to vibrotactile sensitivity and receptive field characteristics into a rapidly adapting (RA) class, sensitive to low frequency (相似文献   

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)     

西伯利亚幼鲟对偶极子电场的避让行为研究

研究利用人工偶极子电场来模拟生物电场刺激, 对西伯利亚幼鲟的电感受能力进行了行为探究。结果显示西伯利亚幼鲟对本实验中的偶极子电场产生躲避行为, 其平均感受阈值在2月龄为(457.532.5) V/cm,3月龄为(29.52.5) V/cm, 7月龄为(101.0) V/cm。这表明西伯利亚鲟鱼的电感受敏感性随个体的发育而增强, 而这可能与电感受器官数量的增加有关(2月龄为2234470, 7月龄为5273523)。     

Temporal analysis of moving DC electric fields in aquatic media

Many aquatic vertebrates can sense the weak electric fields generated by other animals and may also sense geoelectric or electromagnetic phenomena for use in orientation. All these sources generate stationary (dc) fields. In addition, fields from animals are modulated by respiration and other body movements. Since electroreceptors are insensitive to a pure dc field, it has been suggested that the ac modulation carries most of the relevant information for electrosensory animals. However, in a natural situation pure dc fields are rare since any relative movement between source and receiver will transform a dc field into a time varying signal. In this paper, we will describe the properties of such signals and how they are filtered at the first stage of electrosensory information processing in the brain. We will show that the signal perceived by an animal traversing a dc electric field contains all the information necessary to reconstruct the distance to the source and that the signal conditioning algorithms are perfectly adapted to preserve such information.     

Studies of Mechanoreceptors in Skin of the Snout of the Echidna Tachyglossus aculeatus

The echidna Tachyglossus aculeatus, together with the platypus, belongs to the monotremes, a group of mammals with a number of reptilian characteristics. A structure unique to the skin of monotremes is the push rod—a compacted column of epidermal cells that is 20 μm wide and 100 μm long with its tip at the skin surface, and that is able to move relatively independently of adjacent tissue. At the base of each push rod is a cluster of encapsulated nerve endings. Push rods are common in skin of the snout and have been postulated to have a mechanosensory function. Experiments were carried out on four anesthetized echidnas with the aim of determining the function of push rods. Recordings made from the infraorbital nerve, which supplies the skin of the upper jaw, yielded responses from a total of 46 afferents. Two were electroreceptors; the others were mechanoreceptors. Within the group of mechanoreceptors with rapidly adapting responses, three responded to high-frequency vibration and resembled pacinian corpuscles. There were 26 slowly adapting (SA) mechanoreceptors, which, based on the regularity of their discharge, could be divided into two groups: SA I or Merkel type, and SA II or Ruffini type. SA I receptors had very discrete receptive fields with diameters of 100 μm. The receptive fields of two SA I receptors were marked, and after histological processing, one was seen to lie near two push rods. It is concluded that mechanoreceptor responses in the echidna's snout skin resemble those in other mammals in many aspects. We could not unequivocally associate responses to mechanical stimulation with the push rods.     

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.     

Electrosensory ampullary organs are derived from lateral line placodes in cartilaginous fishes

Ampullary organ electroreceptors excited by weak cathodal electric fields are used for hunting by both cartilaginous and non-teleost bony fishes. Despite similarities of neurophysiology and innervation, their embryonic origins remain controversial: bony fish ampullary organs are derived from lateral line placodes, whereas a neural crest origin has been proposed for cartilaginous fish electroreceptors. This calls into question the homology of electroreceptors and ampullary organs in the two lineages of jawed vertebrates. Here, we test the hypothesis that lateral line placodes form electroreceptors in cartilaginous fishes by undertaking the first long-term in vivo fate-mapping study in any cartilaginous fish. Using DiI tracing for up to 70 days in the little skate, Leucoraja erinacea, we show that lateral line placodes form both ampullary electroreceptors and mechanosensory neuromasts. These data confirm the homology of electroreceptors and ampullary organs in cartilaginous and non-teleost bony fishes, and indicate that jawed vertebrates primitively possessed a lateral line placode-derived system of electrosensory ampullary organs and mechanosensory neuromasts.     

Directional characteristics of tuberous electroreceptors in the weakly electric fish,Hypopomus (Gymnotiformes)

This paper is an electrophysiological study of the directionality of the tuberous electroreceptors of weakly electric fish. We recorded from two classes of tuberous electroreceptors known for pulse gymnotiforms: Burst Duration Coders (BDCs), and Pulse Markers (PMs). Both code for stimulus amplitude, although the dynamic range for BDCs is greater, and both exhibit strong directional preferences. Polar plots of spike number (for BDCs) or spike threshold (for PMs) versus electric field azimuth, are figure-8 shaped with two asymmetrical, elliptical lobes separated by 180°. The best azimuth of these two types of receptors from a given body region correlate with each other and with measures of best azimuth for transepidermal current flow. The shape and asymmetry of the directionality profiles appear to be caused by filter dynamics of the receptors. Pulse Markers are located on the anterior part of the body surface while Burst Duration Coders are located all over. The best directions of receptors in the anterior third of the body vary systematically with location from 0° to 180°. This region is probably critical for determining the direction of local electric fields. Together these receptors provide the CNS with sufficient information to construct a map of horizontal plane electric field directions.Abbreviations BDC Burst Duration Coder - ELL electrosensory lateral line lobe - EOD electric organ discharge - nALL anterior lateral line nerve - PM Pulse Marker     

Prey detection mechanism of elasmobranchs

Elasmobranchs can detect a little amount of electric fields and they have characteristic approach strategies to find an electric dipole source generated by prey or conspecifics. They appear to align the body at a constant angle with the current flow line of the electric field while swimming towards prey. However, it has not been studied how they process the perception of electric fields for the approach behaviour or what kind of neural mechanism is used. We use a model of electrosensory perception with electrodynamics and explore a possible approach mechanism based on the sensory landscape distributed on electroreceptors. This paper presents that elasmobranchs can estimate the direction of the electric field by swaying their head, which will be a basis information for their particular approach behaviour. A velocity profile of voltage gradients and intensity difference among the ampullary clusters can be another cues to detect a prey source.     

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 pacemaker 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. Within the torus semicircularis, giant cells are necessary for the performance of the JAR. Giant cell numbers increase exponentially during development and the onset of the JAR coincides with a minimum of at least 150 giant cells and the attainment of a total length of at least 15 mm and at least 150 giant cells. Pacemaker and relay cells comprise the adult Eigenmannia pacemaker nucleus. The growth and differentiation of these cell types also correlates with the onset of the JAR in developing animals. We describe a gradual improvement of sensory abilities, as opposed to an explosive onset of the mature JAR. We further suggest that this may be a rule common in most developing behavioral systems. © 1992 John Wiley & Sons, Inc.     

The Mechanoreceptor Organs of the Lamellirostral Birds (Anseriformes,Aves)

Two types of surface tactile epidermal formations are identified in the bill tip organ of 11 species of lamellirostral birds. Their density arrangement and ratio in the mandible and maxilla are greater in dabbling ducks (filter-feeder species) than in herbivorous and in actively pursuing species. The length and proportions of the connective tissue tubules enclosing the encapsulated mechanoreceptors in filter-feeder species differ significantly from the others. The vibroreceptor endings are significantly more numerous in filter-feeder species and the touch endings in nonfiltering ones. The latter are smaller in the filter-feeder species. Within the walls of the connective tissue tubules, tactile epitheliocytes are registered for the first time. The structure of keratinocytes separating epidermal papillae of the bill tip organ apparently ensures their mobility. The bill tip organ is probably involved in the communication process of waterfowl.     

Orientation processing by synaptic integration across first-order tactile neurons

Our ability to manipulate objects relies on tactile inputs from first-order tactile neurons that innervate the glabrous skin of the hand. The distal axon of these neurons branches in the skin and innervates many mechanoreceptors, yielding spatially-complex receptive fields. Here we show that synaptic integration across the complex signals from the first-order neuronal population could underlie human ability to accurately (< 3°) and rapidly process the orientation of edges moving across the fingertip. We first derive spiking models of human first-order tactile neurons that fit and predict responses to moving edges with high accuracy. We then use the model neurons in simulating the peripheral neuronal population that innervates a fingertip. We train classifiers performing synaptic integration across the neuronal population activity, and show that synaptic integration across first-order neurons can process edge orientations with high acuity and speed. In particular, our models suggest that integration of fast-decaying (AMPA-like) synaptic inputs within short timescales is critical for discriminating fine orientations, whereas integration of slow-decaying (NMDA-like) synaptic inputs supports discrimination of coarser orientations and maintains robustness over longer timescales. Taken together, our results provide new insight into the computations occurring in the earliest stages of the human tactile processing pathway and how they may be critical for supporting hand function.     

From morphology to neural information: the electric sense of the skate

Morphology typically enhances the fidelity of sensory systems. Sharks, skates, and rays have a well-developed electrosense that presents strikingly unique morphologies. Here, we model the dynamics of the peripheral electrosensory system of the skate, a dorsally flattened batoid, moving near an electric dipole source (e.g., a prey organism). We compute the coincident electric signals that develop across an array of the skate's electrosensors, using electrodynamics married to precise morphological measurements of sensor location, infrastructure, and vector projection. Our results demonstrate that skate morphology enhances electrosensory information. Not only could the skate locate prey using a simple population vector algorithm, but its morphology also specifically leads to quick shifts in firing rates that are well-suited to the demonstrated bandwidth of the electrosensory system. Finally, we propose electrophysiology trials to test the modeling scheme.     

Neural mechanisms of tactile motion integration in somatosensory cortex

How are local motion signals integrated to form a global motion percept? We investigate the neural mechanisms of tactile motion integration by presenting tactile gratings and plaids to the fingertips of monkeys, using the tactile analogue of a visual monitor and recording the responses evoked in somatosensory cortical neurons. The perceived directions of the gratings and plaids are measured in parallel psychophysical experiments. We identify a population of somatosensory neurons that exhibit integration properties comparable to those induced by analogous visual stimuli in area MT and find that these neural responses account for the perceived direction of the stimuli across all stimulus conditions tested. The preferred direction of the neurons and the perceived direction of the stimuli can be predicted from the weighted average of the directions of the individual stimulus features, highlighting that the somatosensory system implements a vector average mechanism to compute tactile motion direction that bears striking similarities to its visual counterpart.     

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 GAB-Aergic 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.Abbreviations AENs ascending efferent neurons - GABA gamma-aminobutyric acid     

Effects of fusion between tactile and proprioceptive inputs on tactile perception

Tactile perception is typically considered the result of cortical interpretation of afferent signals from a network of mechanical sensors underneath the skin. Yet, tactile illusion studies suggest that tactile perception can be elicited without afferent signals from mechanoceptors. Therefore, the extent that tactile perception arises from isomorphic mapping of tactile afferents onto the somatosensory cortex remains controversial. We tested whether isomorphic mapping of tactile afferent fibers onto the cortex leads directly to tactile perception by examining whether it is independent from proprioceptive input by evaluating the impact of different hand postures on the perception of a tactile illusion across fingertips. Using the Cutaneous Rabbit Effect, a well studied illusion evoking the perception that a stimulus occurs at a location where none has been delivered, we found that hand posture has a significant effect on the perception of the illusion across the fingertips. This finding emphasizes that tactile perception arises from integration of perceived mechanical and proprioceptive input and not purely from tactile interaction with the external environment.     

Computational Consequences of Temporally Asymmetric Learning Rules: II. Sensory Image Cancellation

The electrosensory lateral line lobe (ELL) of mormyrid electric fish is a cerebellum-like structure that receives primary afferent input from electroreceptors in the skin. Purkinje-like cells in ELL store and retrieve a temporally precise negative image of prior sensory input. The stored image is derived from the association of centrally originating predictive signals with peripherally originating sensory input. The predictive signals are probably conveyed by parallel fibers. Recent in vitro experiments have demonstrated that pairing parallel fiber-evoked excitatory postsynaptic potentials (epsps) with postsynaptic spikes in Purkinje-like cells depresses the strength of these synapses. The depression has a tight dependence on the temporal order of pre- and postsynaptic events. The postsynaptic spike must follow the onset of the epsp within a window of about 60 msec for the depression to occur and pairings at other delays yield a nonassociative enhancement of the epsp. Mathematical analyses and computer simulations are used here to test the hypothesis that synaptic plasticity of the type established in vitro could be responsible for the storage of temporal patterns that is observed in vivo. This hypothesis is confirmed. The temporally asymmetric learning rule established in vitro results in the storage of activity patterns as observed in vivo and does so with significantly greater fidelity than other types of learning rules. The results demonstrate the importance of precise timing in pre- and postsynaptic activity for accurate storage of temporal information.