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Curtis C Bell - One of the best experts on this subject based on the ideXlab platform.
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granular cells of the mormyrid electrosensory lobe and postsynaptic control over presynaptic spike occurrence and amplitude through an electrical synapse
Journal of Neurophysiology, 2007Co-Authors: Jianmei Zhang, Victor Z Han, J Meek, Curtis C BellAbstract:Primary afferent fibers from the Electroreceptors of mormyrid electric fish use a latency code to signal the intensity of electrical current evoked by the fish's own electric organ discharge (EOD)....
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immunocytochemical identification of cell types in the mormyrid electrosensory lobe
The Journal of Comparative Neurology, 2005Co-Authors: Curtis C Bell, J Meek, Jianji Y YangAbstract:The electrosensory lobes (ELLs) of mormyrid and gymnotid fish are useful sites for studying plasticity and descending control of sensory processing. This study used immunocytochemistry to examine the functional circuitry of the mormyrid ELL. We used antibodies against the following proteins and amino acids: the neurotransmitters glutamate and gamma-aminobutyric acid (GABA); the GABA-synthesizing enzyme glutamic acid decarboxylase (GAD); GABA transporter 1; the anchoring protein for GABA and glycine receptors, gephyrin; the calcium binding proteins calbindin and calretinin; the NR1 subunit of the N-methyl-D-aspartate glutamate receptor; the metabotropic glutamate receptors mGluR1alpha, mGluR2/3, and mGluR5; and the intracellular signaling molecules calcineurin, calcium calmodulin kinase IIalpha (CAMKIIalpha) and the receptor for inositol triphosphate (IP3R1alpha). Selective staining allowed for identification of new cell types including a deep granular layer cell that relays sensory information from primary afferent fibers to higher order cells of ELLS. Selective staining also allowed for estimates of relative numbers of different cell types. Dendritic staining of Purkinje-like medium ganglion cells with antibodies against metabotropic glutamate receptors and calcineurin suggests hypotheses concerning mechanisms of the previously demonstrated synaptic plasticity in these cells. Finally, several cell types including the above-mentioned granular cells, thick-smooth dendrite cells, and large multipolar cells of the intermediate layer were present in the two zones of ELL that receive input from mormyromast Electroreceptors but were absent in the zone of ELL that receives input from ampullary Electroreceptors, indicating markedly different processing for these two types of input. J. Comp. Neurol. 483:124-142, 2005. (c) 2005 Wiley-Liss, Inc.
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the mormyromast region of the mormyrid electrosensory lobe i responses to corollary discharge and electrosensory stimuli
Journal of Neurophysiology, 2003Co-Authors: Claudia Mohr, Patrick Roberts, Curtis C BellAbstract:This is the first of two papers on the electrosensory lobe (ELL) of mormyrid electric fish. The ELL is the first stage in the central processing of electrosensory information from Electroreceptors. Cells of the mormyrid ELL are affected at the time of the electric organ discharge (EOD) by two different inputs, EOD-evoked reafferent input from Electroreceptors and corollary discharge input associated with the motor command that elicits the EOD. This first paper examines the intracellular responses of ELL cells to these two different inputs in the region of ELL that receives primary afferent fibers from mormyromast Electroreceptors. Mormyromast Electroreceptors are responsible for active electrolocation. The paper extends previous studies of the mormyrid ELL by describing the physiological responses of cell types, which had been previously identified only morphologically, including: the two types of Purkinje-like medium ganglionic cells, MG1 and MG2; the thick smooth dendrite cells; and the medium fusiform cells. In addition, two previously unrecognized cell types, the large thick smooth dendrite cell and the interzonal cell, are described both morphologically and physiologically for the first time. Finally, new information is provided on the two types of ELL efferent cells, the large ganglionic and large fusiform cells. All cell types, except for the medium fusiform cell, show nonlinear interactions between electrosensory and corollary discharge inputs. All cell types, except for the medium fusiform cell and the interzonal cell, also show plasticity of the corollary discharge response after pairing with electrosensory stimuli.
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nucleus preeminentialis of mormyrid fish a center for recurrent electrosensory feedback i electrosensory and corollary discharge responses
Journal of Neurophysiology, 1996Co-Authors: G Von Der Emde, Curtis C BellAbstract:1. The nucleus preeminentialis (PE) is a large central structure that projects both directly and indirectly to the electrosensory lobe (ELL) where the primary afferents from Electroreceptors terminate. PE receives electrosensory input directly from ELL and also from higher stages of the electrosensory pathway. PE is thus an important part of a central feedback loop that returns electrosensory information from higher stages of the system to the initial stage in ELL. 2. This study describes the field potentials and single-unit activity that are evoked in PE by electrosensory stimuli and by corollary discharge signals associated with the motor command that drives the electric organ to discharge. All recordings were extracellular in this study. 3. Two types of negative-going corollary discharge-evoked field potentials were found in PE: 1) a shallow, long-lasting negative wave with a latency at the peak of approximately 11 ms, and 2) a more sharply falling and larger negative wave with a shorter latency at the peak of approximately 9 ms. The long-latency wave was predominant in the dorsolateral and posterior parts of PE, whereas the short-latency wave was predominant in the medial and rostral regions. Both waves were only found in PE and thus can serve for its identification. 4. Electrosensory stimuli given either locally to a restricted skin region or symmetrically to the entire body evoked characteristic field potentials in both regions of PE. The mean latency between the stimulus and the peak of the response was 6.9 ms in the early negativity region and 12.2 ms in the late negative region. The responses to such stimuli were strongly facilitated by the electric organ corollary discharge. 5. Field potential responses to the electric organ corollary discharge were markedly plastic. Responses to the corollary discharge plus a paired electrosensory stimulus decreased over time and the response to the corollary discharge alone was markedly enhanced after a period of such pairing. 6. Local electrosensory stimulation of the skin showed that the caudal-rostral body axis is mapped from dorsal-medial to ventral-lateral in PE. The same somatotopy was found in the regions of the early and late negatives. The ventral and dorsal body appeared not to be separately mapped in PE. The areas representing the head and chin appendage ("Schnauzenorgan") are especially large in PE, due presumably to the high density of Electroreceptors in these areas. 7. Two main types of units were recorded in PE: 1) inhibitory (I) cells with a corollary discharge response that was inhibited by an electrosensory stimulus to the center of their receptive fields; and 2) excitatory (E) cells with an excitatory response to electrosensory stimuli that was facilitated by the corollary discharge. Some of the E cells responded to the corollary discharge alone and some did not. Most cells appeared to be responding to input from mormyromast Electroreceptors, but a few cells were driven by ampullary Electroreceptors and a few by Knollenorgan Electroreceptors. 8. The corollary discharge effects on I cells and E cells were plastic and depended on previous pairing with a sensory stimulus. The corollary discharge facilitation of E cells and inhibition of I cells decreased during pairing with a sensory stimulus, and the corollary discharge-driven excitation of I cells was much larger after pairing than before. 9. The results provide an initial overview of a major component in the control of electrosensory information processing by recurrent feedback from higher stages of the system.
Jan Benda - One of the best experts on this subject based on the ideXlab platform.
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Chapter 12 Neural Noise in Electrocommunication — From Burden to Benefits
2015Co-Authors: Jan Benda, Jan GreweAbstract:use for active electrosensation. This system is used for both object localisation and electro-communication. Both, objects that are close to the fish and the EODs of other nearby electric fish, modulate the amplitude of a fish’s EOD. Localisation signals are low in amplitude and fre-quency whereas electrocommunication signals are large amplitude signals with higher frequen-cies. Electroreceptor neurons are tuned to the frequency of the fish’s own EOD. This tuning, however, is rather broad to allow for reception of EODs of other fish with different frequencies. This is the basis for electrocommunication. Spike trains of Electroreceptor afferents are sur-prisingly noisy even in the absence of any external signal. From theoretical studies it is known that in populations of spiking neurons such internal noise can improve the information carried about a common input signal in comparison to the noiseless case. In particular, the processing of high-frequency signals benefits from internal noise and the convergence of large populations of neurons. The target neurons of the Electroreceptor afferents, the pyramidal cells in the elec-trosensory lateral line lobe, are organised in three distinct maps of the electroreceptive body surface that are characterised by different receptive field sizes, i.e. the number of afferents that converge on them, and frequency tuning. The properties of these three maps can be understoo
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Behavioral/Systems/Cognitive Spike-Frequency Adaptation Separates Transient Communication Signals from Background Oscillations
2014Co-Authors: Jan Benda, André LongtinAbstract:Spike-frequency adaptation is a prominent feature ofmany neurons. However, little is known about its computational role in processing behaviorally relevant natural stimuli beyond filtering out slow changes in stimulus intensity. Here, we present a more complex example in whichwe demonstrate how spike-frequency adaptation plays a key role in separating transient signals from slower oscillatory signals. We recorded in vivo from very rapidly adapting Electroreceptor afferents of the weakly electric fish Apteronotus leptorhynchus. The firing-frequency response of Electroreceptors to fast communication stimuli (“small chirps”) is strongly enhanced compared with the response to slower oscillations (“beats”) arising from interactions of same-sex conspecifics. We are able to accurately predict the elec-troreceptor afferent response to chirps and beats, using a recently proposed general model for spike-frequency adaptation. The param-eters of themodel are determined for each neuron individually from the responses to step stimuli. We conclude that the dynamics of the rapid spike-frequency adaptation is sufficient to explain the data. Analysis of additional data from step responses demonstrates that spike-frequency adaptation acts subtractively rather than divisively as expected from depressing synapses. Therefore, the adaptation dynamics is linear and creates a high-pass filter with a cutoff frequency of 23 Hz that separates fast signals from slower changes in input. A similar critical frequency is seen in behavioral data on the probability of a fish emitting chirps as a function of beat frequency. These results demonstrate how spike-frequency adaptation in general can facilitate extraction of signals of different time scales, specifically high-frequency signals embedded in slower oscillations. Key words: adaptation; high-pass filter; communication; receptor neuron; electrosensory system; weakly electric fis
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the effect of difference frequency on electrocommunication chirp production and encoding in a species of weakly electric fish apteronotus leptorhynchus
Journal of Physiology-paris, 2008Co-Authors: Ginette J Hupe, John E. Lewis, Jan BendaAbstract:The brown ghost knifefish, Apteronotus leptorhynchus, is a model wave-type gymnotiform used extensively in neuroethological studies. As all weakly electric fish, they produce an electric field (electric organ discharge, EOD) and can detect electric signals in their environments using Electroreceptors. During social interactions, A. leptorhynchus produce communication signals by modulating the frequency and amplitude of their EOD. The Type 2 chirp, a transient increase in EOD frequency, is the most common modulation type. We will first present a description of A. leptorhynchus chirp production from a behavioural perspective, followed by a discussion of the mechanisms by which chirps are encoded by Electroreceptor afferents (P-units). Both the production and encoding of chirps are influenced by the difference in EOD frequency between interacting fish, the so-called beat or difference frequency (Df). Chirps are produced most often when the Df is small, whereas attacks are more common when Dfs are large. Correlation analysis has shown that chirp production induces an echo response in interacting conspecifics and that chirps are produced when attack rates are low. Here we show that both of these relationships are strongest when Dfs are large. Electrophysiological recordings from Electroreceptor afferents (P-units) have suggested that small, Type 2 chirps are encoded by increases in Electroreceptor synchrony at low Dfs only. How Type 2 chirps are encoded at higher Dfs, where the signals seem to exert the greatest behavioural influence, was unknown. Here, we provide evidence that at higher Dfs, chirps could be encoded by a desynchronization of the P-unit population activity.
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A synchronization-desynchronization code for natural communication signals. Neuron 52
2006Co-Authors: Jan Benda, André Longtin, Leonard MalerAbstract:Synchronous spiking of neural populations is hypothesized to play important computational roles in forming neural assemblies and solving the binding problem. Although the opposite phenomenon of desynchronization is well known from EEG studies, it is largely neglected on the neuronal level. We here provide an example of in vivo recordings from weaklyelectric fish demonstrating that, depending on the social context, different types of natural communication signals elicit transient desynchronization as well as synchronization of the Electroreceptor population without changing the mean firing rate. We conclude that, in general, both positive and negative changes in the degree of synchrony can be the relevant signals for neural information processing
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Spike-frequency adaptation separates transient communication signals from background oscillations
2005Co-Authors: Jan Benda, André Longtin, Len MalerAbstract:Spike-frequency adaptation is a prominent feature of many neurons. However, little is known about its computational role in processing behaviorally relevant natural stimuli beyond filtering out slow changes in stimulus intensity. Here we present a more complex example where we demonstrate how spike-frequency adaptation plays a key role in separating transient signals from slower oscillatory signals. We recorded in vivo from very rapidly adapting Electroreceptor afferents of the weakly electric fish Apteronotus leptorhynchus. The firing-frequency response of Electroreceptors to fast communication stimuli (“small chirps”) is strongly enhanced compared to the response to slower oscillations (“beats”) arising from interactions of same-sex conspecifics. We are able to accurately predict the Electroreceptor afferent response to chirps and beats, using a recently proposed general model for spike-frequency adaptation. The model’s parameters are determined for each neuron individually from the responses to step stimuli. We conclude that the dynamics of the rapid spike-frequency adaptation is sufficient to explain the data. Analysis of additional data from step-responses demonstrates that spike frequency adaptation acts subtractively rather than divisively as expected from depressing synapses. Therefore, the adaptation dynamics is linear and creates a high-pass filter with a cutoff frequency of 23 Hz that separates fast signals from slower changes in input. A similar critical frequency is seen in behavioral data on the probability of a fish emitting chirps as a function of beat frequency. These results demonstrate how spike-frequency adaptation in general can facilitate extraction of signals of different time scales, specifically high-frequency signals embedded in slower oscillations. 1 Jan Benda et al.: Temporal Signal Separation by Neural Adaptation
Shaun P. Collin - One of the best experts on this subject based on the ideXlab platform.
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The distribution and abundance of electrosensory pores in two benthic sharks: A comparison of the wobbegong shark, Orectolobus maculatus, and the angel shark, Squatina australis
Marine and Freshwater Research, 2014Co-Authors: Channing A. Egeberg, Ryan M Kempster, Susan M. Theiss, Nathan S. Hart, Shaun P. CollinAbstract:Electroreception is an ancient sense found in many aquatic animals, including sharks, which may be used in the detection of prey, predators and mates. Wobbegong sharks (Orectolobidae) and angel sharks (Squatinidae) represent two distantly related families that have independently evolved a similar dorso-ventrally compressed body form to complement their benthic ambush feeding strategy. Consequently, these groups represent useful models in which to investigate the specific morphological and physiological adaptations that are driven by the adoption of a benthic lifestyle. In this study, we compared the distribution and abundance of electrosensory pores in the spotted wobbegong shark (Orectolobus maculatus) with the Australian angel shark (Squatina australis) to determine whether both species display a similar pattern of clustering of sub-dermal Electroreceptors and to further understand the functional importance of electroreception in the feeding behaviour of these benthic sharks. Orectolobus maculatus has a more complex electrosensory system than S. australis, with a higher abundance of pores and an additional cluster of Electroreceptors positioned in the snout (the superficial ophthalmic cluster). Interestingly, both species possess a cluster of pores (the hyoid cluster, positioned slightly posterior to the first gill slit) more commonly found in rays, but which may be present in all benthic elasmobranchs to assist in the detection of approaching predators.
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survival of the stillest predator avoidance in shark embryos
PLOS ONE, 2013Co-Authors: Ryan M Kempster, Nathan S. Hart, Shaun P. CollinAbstract:Sharks use highly sensitive Electroreceptors to detect the electric fields emitted by potential prey. However, it is not known whether prey animals are able to modulate their own bioelectrical signals to reduce predation risk. Here, we show that some shark (Chiloscyllium punctatum) embryos can detect predator-mimicking electric fields and respond by ceasing their respiratory gill movements. Despite being confined to the small space within the egg case, where they are vulnerable to predators, embryonic sharks are able to recognise dangerous stimuli and react with an innate avoidance response. Knowledge of such behaviours, may inform the development of effective shark repellents.
G Von Der Emde - One of the best experts on this subject based on the ideXlab platform.
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active electroreception vertebrates
Encyclopedia of Animal Behavior, 2010Co-Authors: G Von Der EmdeAbstract:Weakly electric fish emit electric signals with an electric organ in their tail and perceive them with cutaneous Electroreceptor organs. During active electrolocation, objects are detected and analyzed because they distort the self-produced electrical field and project electric images onto the electroreceptive skin surface. To optimize electrical imaging of the environment, the fish perform certain electromotor and locomotor behaviors (probing motor acts). For fine spatial analysis, the mormyrid Gnathonemus petersii focuses electric images of objects onto two ‘foveal’ skin regions: the ‘Schnauzenorgan’ and the ‘nasal region.’ Sudden emergences of novel stimuli evoke the so-called novelty responses (electromotor) and Schnauzenorgan responses (movements of the chin).
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distribution density and morphology of Electroreceptor organs in mormyrid weakly electric fish anatomical investigations of a receptor mosaic
Journal of Zoology, 2008Co-Authors: Michael Hollmann, Jacob Engelmann, G Von Der EmdeAbstract:Gnathonemus petersii and other African weakly electric fish (Mormyridae) produce electric signals in order to sense their environment, a process called active electrolocation. During active electrolocation electrical images of objects in the environment are cast onto a mosaic of Electroreceptors, which are embedded in the animal's skin. In Gn. petersii and four other species of mormyrid fish, the densities of Electroreceptor organs (mormyromasts and ampullary organs) were determined at various skin regions, including the chin, the nasal region and the back. In all species investigated, the highest mormyromast densities were found at the chin, followed by the nasal region. In addition to this comparative approach, we investigated the electroreceptive epidermis of Gn. petersii in more detail. At the moveable chin appendix, the Schnauzenorgan, scanning electron microscopy analysis helped to elucidate the mosaic-like distribution and the morphology of the Electroreceptor organs and their embedding in the epidermis. Because the number of mormyromasts increased very little when fish got bigger, receptor organ densities decreased with standard length. Mormyromast density at the Schnauzenorgan, especially at its tip, highly exceeded that at all other skin regions. Along the Schnauzenorgan, receptor densities decreased exponentially from the tip towards the base. At the nasal region, mormyromast densities were more than three times higher compared to the rest of the fish's head and trunk. A similar distribution to that of the mormyromasts was found for the ampullary Electroreceptor organs, which are used for passive electroreception. Our findings support the hypothesis that at least in Gn. petersii the Schnauzenorgan and the nasal region are electroreceptive foveae.
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nucleus preeminentialis of mormyrid fish a center for recurrent electrosensory feedback i electrosensory and corollary discharge responses
Journal of Neurophysiology, 1996Co-Authors: G Von Der Emde, Curtis C BellAbstract:1. The nucleus preeminentialis (PE) is a large central structure that projects both directly and indirectly to the electrosensory lobe (ELL) where the primary afferents from Electroreceptors terminate. PE receives electrosensory input directly from ELL and also from higher stages of the electrosensory pathway. PE is thus an important part of a central feedback loop that returns electrosensory information from higher stages of the system to the initial stage in ELL. 2. This study describes the field potentials and single-unit activity that are evoked in PE by electrosensory stimuli and by corollary discharge signals associated with the motor command that drives the electric organ to discharge. All recordings were extracellular in this study. 3. Two types of negative-going corollary discharge-evoked field potentials were found in PE: 1) a shallow, long-lasting negative wave with a latency at the peak of approximately 11 ms, and 2) a more sharply falling and larger negative wave with a shorter latency at the peak of approximately 9 ms. The long-latency wave was predominant in the dorsolateral and posterior parts of PE, whereas the short-latency wave was predominant in the medial and rostral regions. Both waves were only found in PE and thus can serve for its identification. 4. Electrosensory stimuli given either locally to a restricted skin region or symmetrically to the entire body evoked characteristic field potentials in both regions of PE. The mean latency between the stimulus and the peak of the response was 6.9 ms in the early negativity region and 12.2 ms in the late negative region. The responses to such stimuli were strongly facilitated by the electric organ corollary discharge. 5. Field potential responses to the electric organ corollary discharge were markedly plastic. Responses to the corollary discharge plus a paired electrosensory stimulus decreased over time and the response to the corollary discharge alone was markedly enhanced after a period of such pairing. 6. Local electrosensory stimulation of the skin showed that the caudal-rostral body axis is mapped from dorsal-medial to ventral-lateral in PE. The same somatotopy was found in the regions of the early and late negatives. The ventral and dorsal body appeared not to be separately mapped in PE. The areas representing the head and chin appendage ("Schnauzenorgan") are especially large in PE, due presumably to the high density of Electroreceptors in these areas. 7. Two main types of units were recorded in PE: 1) inhibitory (I) cells with a corollary discharge response that was inhibited by an electrosensory stimulus to the center of their receptive fields; and 2) excitatory (E) cells with an excitatory response to electrosensory stimuli that was facilitated by the corollary discharge. Some of the E cells responded to the corollary discharge alone and some did not. Most cells appeared to be responding to input from mormyromast Electroreceptors, but a few cells were driven by ampullary Electroreceptors and a few by Knollenorgan Electroreceptors. 8. The corollary discharge effects on I cells and E cells were plastic and depended on previous pairing with a sensory stimulus. The corollary discharge facilitation of E cells and inhibition of I cells decreased during pairing with a sensory stimulus, and the corollary discharge-driven excitation of I cells was much larger after pairing than before. 9. The results provide an initial overview of a major component in the control of electrosensory information processing by recurrent feedback from higher stages of the system.
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the sensing of electrical capacitances by weakly electric mormyrid fish effects of water conductivity
The Journal of Experimental Biology, 1993Co-Authors: G Von Der EmdeAbstract:Summary Weakly electric fish can perceive electric properties of objects by monitoring the responses of their epidermal Electroreceptors (mormyromasts) to their own electric organ discharges (EOD), a process known as active electrolocation. Mormyrid fish can distinguish capacitative from resistive properties of objects. It is mainly animate objects that possess capacitative properties. Water conductivity is a critical environmental factor that varies widely from season to season and has strong effects on the emitted EOD. The two goals of this study were: (1) to investigate the ability of Gnathonemus petersii to detect the properties of capacitative objects in waters of different ion content and (2) to test a recently formulated hypothesis which states that the detection of the features of a capacitative object depends on a comparison of the inputs from the two types of mormyromast primary afferents. Individuals of G. petersii were tested in a conditioned electrolocation procedure. With increasing water conductivities from 50 to 1100 mS cm 21 , EOD amplitude decreased and the detection threshold for small capacitances increased. At 50 mS cm 21 , the smallest detectable capacitative value was below 0.5nF; this increased to about 20nF at 800 mS cm 21 . When conductivity approached about 1000 mS cm 21 , fish were no longer able to electrolocate , probably because of the reduction in EOD amplitude at high conductivities. The fish’s ability to discriminate a capacitative object unequivocally from every resistive object was also tested at different conductivities. Below about 800 mS cm 21 , all fish could do so. Above that conductivity, however, fish could no longer discriminate between capacitative and resistive objects of similar impedance, although they could still discriminate between objects of different impedances. The two types of receptor afferents (from the ‘A’ and ‘B’ cells) of mormyromast Electroreceptor organs have different thresholds, with the B afferents being more sensitive. I suggest that only the B receptor cells remain active at about 800 mS cm 21 , when the EOD amplitude is much reduced. With input from B afferents only, an unambiguous capacitance detection was no longer possible. This supports the hypothesis that capacitance detection is achieved by comparing inputs of A and B Electroreceptor cells.
John D. Pettigrew - One of the best experts on this subject based on the ideXlab platform.
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22 and platypus parallel evolution of passive electroreception in a rostral bill organ
2002Co-Authors: John D. Pettigrew, Lon A WilkensAbstract:A comparison is made between a mammalian, monotreme species and an actinopterygian fish that have each, indepen dently, evolved a similar, spoonbill-shaped rostral bill organ whose array of Electroreceptors provides sufficient spatial information for prey capture in a freshwater environment without the need for visual cues. The platypus, Ornithorhyncus anatinus (Monotremata, Mammalia), has approximately 40,000 Electroreceptors arranged in parasagittal rows on the bill organ. By means of behavioral and electrophysiological recording experiments in platypus, it has been shown that this array of Electroreceptors can trigger an accurately directed head saccade to intersect aquatic prey that emit electrical signals. The threshold field strength for prey detection by platypus signals is 50 microvolts/cm, two orders of magnitude more sensitive than individual Electroreceptors. The paddlefish, Polyodon spathula (Osteichthyes, Actinopterygii), can similarly execute a lateral head saccade to intersect prey, with a threshold field strength around 10 microvolts/cm, considerably more sensitive than the presumed sensitivity of individual Electroreceptors. The remarkable anatomical and behavioral similarities between these two independent electroreceptive systems are described and discussed. Major differences between the two bill-organ systems include the mechanism of transduction at the Electroreceptors and a prominent cooperative role played by 60,000 mechanoreceptors that are interdigitated among the Electroreceptors in the platypus bill but not in the paddlefish.
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distribution and putative function of autonomic nerve fibres in the bill skin of the platypus ornithorhynchus anatinus
Philosophical Transactions of the Royal Society B, 1998Co-Authors: Paul R. Manger, John D. Pettigrew, Janet R Keast, Louise TrouttAbstract:The Electroreceptors located in the bill skin of the platypus are modified secretory glands. The electroreceptive nerve terminals form bare endings in close proximity to the duct of these glands. In this study, we describe the autonomic innervation of the glands and a separate specialized autonomic innervation of the epidermal portion of the glandular duct. A range of immunohistochemical labels showed that the gland cells of the Electroreceptors have a non-noradrenergic (putative parasympathetic) innervation. Phalloidin labelling revealed a 'sphincter' of epidermal luminal cells that labelled strongly for actin. These actin-dense keratinocytes were seen to have a noradrenergic (putative sympathetic) innervation. Fine-diameter sensory fibres containing substance P (presumably C-fibre thermoreceptors or polymodal nociceptors) were observed to terminate in the superficial epidermis surrounding the pore of the gland. When the bill of the platypus is dry these pores were closed. However, when room temperature water was washed over the bill, the pores opened. It is proposed that this autonomic and sensory innervation, along with the actin sphincter, mediates the opening and closing of the pores. By doing this, the platypus prevents the desiccation of the bare electrosensory nerve terminals when it is out of the water, and it may also be a way to regulate the impedance of the internal electrical circuit presented to the water at the pores.
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ultrastructure number distribution and innervation of Electroreceptors and mechanoreceptors in the bill skin of the platypus ornithorhynchus anatinus
Brain Behavior and Evolution, 1996Co-Authors: Paul R. Manger, John D. PettigrewAbstract:The platypus is presently the only mammal demonstrated to use electroreception to obtain food. The electroreceptive system of the platypus is far more complex than that of its close relative the echidna. This paper presents an anatomical study of the basis of electroreception in the platypus. The innervation of the bill by the trigeminal nerve is described, as are three sensory structures, associated with food gathering, within the bill skin. There are 40,000 mucous gland Electroreceptors found in the bill skin of the platypus. The papillary portion of each of these sensory mucous glands is modified to accommodate electrosensory nerve terminals. In contrast to fish Electroreceptors, the electrosensory terminals of the platypus are not associated with a sensory cell. These mucous gland Electroreceptors are arranged in a series of parasagittal stripes on the bill. This array suggests a basis for the ability of the platypus to quickly and accurately locate the origin of an electrical stimulus. A push-rod mechanoreceptor, similar in morphology to Eimer's organ of the mole, and bill-tip organs in birds, was also found in the bill skin. The slightly differing morphology of these mechanoreceptors when compared to their avian and talpid counterparts suggests that this is another example of convergent evolution, with the common need to provide a solution to increasing tactile sensitivity on bare rhinarial skin. These push-rods are found to be most dense around the labial margins of the bill, with a marked decrease in density towards the middle and caudal portions of the bill. The distribution of the push-rods is similar to the distribution of the third sensory structure found on the bill, the sensory serous gland. Although less numerous than the mechanoreceptors (46,500 mechanoreceptors compared with 13,500 sensory serous glands), these sensory serous glands have a similar distribution and similar changes in density. These concurrent distributions argue for some functional correlation of these two sensory structures. The papillary region of the serous gland is modified in a manner similar to that of the mucous gland Electroreceptor to accommodate sensory input. The sensory terminals of the serous glands are very similar to those of the mucous gland Electroreceptors, and so it is presumed that these sensory serous glands are a type of Electroreceptor that might be involved in detection of electrical signals at close quarters where the mechanorecemors are also engaged.
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nerve terminals of mucous gland Electroreceptors in the platypus ornithorhynchus anatinus
Proceedings of The Royal Society B: Biological Sciences, 1995Co-Authors: Paul R. Manger, John D. Pettigrew, Janet R Keast, Amanda BauerAbstract:Platypus mucous gland Electroreceptors differ from Electroreceptors described for fish in that they lack an associated specialized sensory cell. Thus a bare nerve terminal is used to detect electrical stimuli, and also to generate local and action potentials. Previous studies have identified these terminals (an average of 16 per mucous gland), but had not shown whether the terminals have direct contact with the duct of the mucous gland. This poses the problem of how the electrical stimulus reaches the nerve terminals. This study demonstrates the portions of the nerve terminals responsible for electroreception, and shows how these portions use the surrounding epidermal tissue to overcome the combined problems of lacking a sensory cell and making physical contact with the conducting medium in the duct of the gland. A terminal axonal filament is described which accommodates for these problems, the terminal filament provides a low-resistance pathway for the electrical stimuli, and is embedded with its proximal and distal portions in high and low resistance epidermis, respectively. Lateral interactions occur between adjacent terminal filaments via a plexus that is directed circumferentially around the duct from the proximal portion of the terminal filament. These circumferential arbors form an interconnecting ring between all 16 terminal filaments, and may be used to lower the signal-to-noise ratio of the Electroreceptor and thus enhance overall sensitivity.