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J D Pettigrew

Publications and source records attributed to J D Pettigrew.

At least 37 records · Page 2Linked to original sources
PubMed1998

Monotremes and the evolution of rapid eye movement sleep.

Early studies of the echidna led to the conclusion that this monotreme did not have rapid eye movement (REM) sleep. Because the monotremes had diverged from the placental and marsupial lines very early in mammalian evolution, this finding was used to support the hypothesis that REM sleep evolved after the start of the mammalian line. The current paper summarizes our recent work on sleep in the echidna and platypus and leads to a very different interpretation. By using neuronal recording from mesopontine regions in the echidna, we found that despite the presence of a high-voltage cortical electroencephalogram (EEG), brainstem units fire in irregular bursts intermediate in intensity between the regular non-REM sleep pattern and the highly irregular REM sleep pattern seen in placentals. Thus the echidna displays brainstem activation during sleep with high-voltage cortical EEG. This work encouraged us to do the first study of sleep, to our knowledge, in the platypus. In the platypus we saw sleep with vigorous rapid eye, bill and head twitching, identical in behaviour to that which defines REM sleep in placental mammals. Recording of the EEG in the platypus during natural sleep and waking states revealed that it had moderate and high-voltage cortical EEGs during this REM sleep state. The platypus not only has REM sleep, but it had more of it than any other animal. The lack of EEG voltage reduction during REM sleep in the platypus, and during the REM sleep-like state of the echidna, has some similarity to the sleep seen in neonatal sleep in placentals. The very high amounts of REM sleep seen in the platypus also fit with the increased REM sleep duration seen in altricial mammals. Our findings suggest that REM sleep originated earlier in mammalian evolution than had previously been thought and is consistent with the hypothesis that REM sleep, or a precursor state with aspects of REM sleep, may have had its origin in reptilian species.

Animals↗
PubMed1998

Distribution and putative function of autonomic nerve fibres in the bill skin of the platypus (Ornithorhynchus anatinus).

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.

Actins↗
PubMed1998

The development of the electroreceptors of the platypus (Ornithorhynchus anatinus).

A series of developmental stages of the platypus were examined to obtain an anatomical description of the development of the periphery of the electroreceptive system. Putative electroreceptors, composed of modified mucous glands, were observed to appear at 10 days post hatching (p.h.). The typical striped arrangement of peripheral electroreceptors in the platypus was seen at 12 days p.h. The arrangement of the stripes was modified during development with a range of additions and divisions of stripes occurring until the adult pattern is obtained, approximately 6 months p.h. After appearing at 10 days p.h., the number of electroreceptors increases rapidly until sometime between 24 and 28 days p.h. when there is massive death of electroreceptors, the number present at 28 days p.h. being 60% of the number present at 24 days p.h. This massive death of receptors is coincident with the appearance of other sensory structures in the epidermis of the bill skin, the push-rod mechanoreceptors and the sensory serous glands. Histological examination of a range of developmental stages demonstrated poorly differentiated innervation at 28 days p.h., which became differentiated and reached the adult configuration between 11 weeks p.h. and 6 months p.h., the time at which nestling platypuses leave the burrow. Lamination of the cells lining the duct of the electroreceptors showed a similar developmental profile. This study indicates that the electroreceptive system of the developing platypus is not functional, in a similar manner to the adult, until it is time for the platypus to leave the nesting burrow. However, the system may be functional in the developing platypus, and may be used speculatively in the location of the mammary region for suckling.

Animals↗
PubMed1998

The sensory world of the platypus.

Vision, audition and somatic sensation in the platypus are reviewed. Recent work on the eye and retinal ganglion cell layer of the platypus is presented that provides an estimate of visual acuity and suggests that platypus ancestors may have used vision, as well as the bill organ, for underwater predation. The combined electroreceptor and mechanoreceptor array in the bill is considered in detail, with special reference to the elaborate cortical structure, where inputs from these two sensory arrays are integrated in a manner that is astonishingly similar to the stripe-like ocular dominance array in primate visual of cortex, that integrates input from the two eyes. A new hypothesis, along with supporting data, is presented for this combined mechanoreceptive-electroreceptive complex in platypus cortex. Bill mechanoreceptors are shown to be capable of detecting mechanical waves travelling through the water from moving prey. These mechanical waves arrive after the electrical activity from the same prey, as a function of distance. Bimodal cortical neurones, sensitive to combined mechanical and electrical stimulation, with a delay, can thus signal directly the absolute distance of the prey. Combined with the directional information provided by signal processing of the thousands of receptors on the bill surface, the stripe-like cortical array enables the platypus to use two different sensory systems in its bill to achieve a complete, three-dimensional 'fix' on its underwater prey.

Animals↗
PubMed1998

Some related aspects of platypus electroreception: temporal integration behaviour, electroreceptive thresholds and directionality of the bill acting as an antenna.

This paper focuses on how the electric field from the prey of the platypus is detected with respect to the questions of threshold determination and how the platypus might localize its prey. A new behaviour in response to electrical stimuli below the thresholds previously reported is presented. The platypus shows a voluntary exploratory behaviour that results from a temporal integration of a number of consecutive stimulus pulses. A theoretical analysis is given, which includes the threshold dependence on the number of receptors and temporal integration of consecutive stimuli pulses, the close relationships between electrical field decay across the bill, electroreceptive thresholds and directionality of the platypus bill acting as an antenna. It is shown that a lobe shape, similar to that which has been measured, can be obtained by combining responses in a specific way from receptors sensing the electric field decay across the bill. Two possible methods for such combinations are discussed and analysed with respect to measurements and observed behaviour of the platypus. A number of factors are described which need to be considered when electroreceptive thresholds are to be determined. It is shown that some information about the distance to the source is theoretically available from the pattern of field decay across the platypus's bill. The paper includes a comparative analysis of radar target tracking and platypus prey localization.

Animals↗
PubMed1998

Base-compositional biases and the bat problem. III. The questions of microchiropteran monophyly.

Using single-copy DNA hybridization, we carried out a whole genome study of 16 bats (from ten families) and five outgroups (two primates and one each dermopteran, scandentian, and marsupial). Three of the bat species represented as many families of Rhinolophoidea, and these always associated with the two representatives of Pteropodidae. All other microchiropterans, however, formed a monophyletic unit displaying interrelationships largely in accord with current opinion. Thus noctilionoids comprised one clade, while vespertilionids, emballonurids, and molossids comprised three others, successively more closely related in that sequence. The unexpected position of rhinolophoids may be due either to the high AT bias they share with pteropodids, or it may be phylogenetically authentic. Reanalysis of the data with varying combinations of the five outgroups does not indicate a rooting problem, and the inclusion of many bat lineages divided at varying levels similarly discounts long branch attraction as an explanation for the pteropodid-rhinolophoid association. If rhinolophoids are indeed specially related to pteropodids, many synapomorphies of Microchiroptera are called into question, not least the unitary evolution of echolocation (although this feature may simply have been lost in pteropodids). Further, a rhinolophoid-pteropodid relationship--if true--has serious implications for the classification of bats. Finally, among the outgroups, an apparent sister-group relation of Dermoptera and Primates suggests that flying lemurs do not represent the ancestors of some or all bats; yet, insofar as gliding of the type implemented in dermopterans is an appropriate model for the evolution of powered mammalian flying, the position of Cynocephalus in our tree indirectly strengthens the argument that true flight could have evolved more than once among bats.

Animals↗
PubMed1998

Base-compositional biases and the bat problem. I. DNA-hybridization melting curves based on AT- and GC-enriched tracers.

We explored the interordinal relationships of mammals using DNA-DNA hybridization, with particular reference to the much-debated problem of whether the megabats and microbats are more closely related to each other than the megabats are to primates. To try to improve resolution when taxa are distantly related and the melting points of hybrids are low and difficult to distinguish, we increased the GC content of DNA by a fractionation method that used the same melting-point apparatus used in the hybridization studies. When we used GC-rich DNA as the tracer to make hybrids, the melting point of the self-hybrid shifted to a higher temperature as expected, but the behaviour of heterologous hybrids varied with the taxa being compared. When the melting point of the heterologous hybrid also shifted to a higher temperature so that the two compared taxa maintained the same or proportional distance, we called this 'following behaviour', because the heterologous hybrid made with GC-rich tracer 'followed' the GC-rich self-hybrid to higher temperatures. We also commonly saw anomalous behaviour, where the melting point of the heterologous hybrid shifted to a lower temperature when compared with an AT-rich hybrid. In these anomalous cases, the distance measured between the taxa increased markedly as a result of GC-enrichment, indicating that an underestimate of distance may have resulted from AT bias in DNA. This inference was supported by the finding that it was rare to observe a decrease in measured distance between taxa using GC-rich DNA, but very common to find an increase as would be expected from the generally higher AT contents of eutherian DNAs. Moreover, the most extreme cases, where distances changed most using GC-rich DNA, were usually those involving comparisons between taxa known to have the most extreme AT-biases among mammals, such as the megabats and rhinolophoid (including megadermatid) microbats. Our results show consistent underestimates of measured differences between eutherian taxa with extreme AT-biases.

Animals↗
PubMed1998

Base-compositional biases and the bat problem. II. DNA-hybridization trees based on AT- and GC-enriched tracers.

We conducted a series of parallel DNA-hybridization experiments on a small group of bats (species of Pteropus, Rhinolophus, Noctilio and Pteronotus) and outgroups (Lemur, Cynocephalus, Didelphis), using whole-genome labels and tracers made from extracts enriched with AT and two levels of GC content. FITCH (additive phylogenetic trees) topologies were constructed from the four sets of comparisons, indexed as both delta Tmode and delta NPHs (normalized percentage of hybridization). Based on our previous work showing that the shared AT bias of pteropodids and some microchiropterans may affect the rank-ordering of taxa based on either AT- or GC-rich labels, our expectation was that the resulting trees would show differing topologies when generated from tracers made with the variously enriched DNA extracts. Whereas there was some variation among the trees, most of them grouped the bats together, and almost all paired the representative megachiropteran and rhinolophoid microchiropteran as sister-taxa in contrast to the other microchiropterans. As the pteropodid-rhinolophoid relationship is an unexpected and unlikely one, we attribute this association to an AT bias that was not obviated even by our most GC-rich labels, and suggest that such a bias may compromise the truth of some molecular trees. Accordingly, we believe the broader issue of bat monophyly remains unresolved by DNA-hybridization and probably also by gene-sequencing studies.

Animals↗
PubMed1996

The echidna Tachyglossus aculeatus combines REM and non-REM aspects in a single sleep state: implications for the evolution of sleep.

Placental and marsupial mammals exist in three states of consciousness: waking, non-REM sleep, and REM sleep. We now report that the echidna Tachyglossus aculeatus, a representative of the earliest branch of mammalian evolution (the monotremes), does not have the pattern of neuronal activity of either of the sleep states seen in nonmonotreme mammals. Echidna sleep was characterized by increased brainstem unit discharge variability, as in REM sleep. However, the discharge rate decreased and the EEG was synchronized, as in non-REM sleep. Our results suggest that REM and non-REM sleep evolved as a differentiation of a single, phylogenetically older sleep state. We hypothesize that the physiological changes that occur during postnatal sleep development parallel certain aspects of the changes that have occurred during the evolution of sleep-waking states in mammals.

Animals↗
PubMed1996

Ultrastructure, number, distribution and innervation of electroreceptors and mechanoreceptors in the bill skin of the platypus, Ornithorhynchus anatinus.

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 mechanoreceptors are also engaged.

Animals↗
PubMed1996

Unusual pattern of retinogeniculate projections in the controversial primate Tarsius.

Studies of simian and prosimian primates have demonstrated a remarkable interspecific constancy in the pattern of innervation of the magnocellular and parvocellular layers of the dorsal lateral geniculate nucleus (dLGN) by retinal afferents. The characteristic organization of this nucleus in primates, as well as its apparent phylogenetic stability, have led to the proposal that the distinct laminar arrangement of the dLGN is one of the diagnostic characters that define the Order Primates. Here, we describe the distribution of retinal afferents to the dLGN of Tarsius, the single contemporary member of an ancient lineage of primates. In this genus, the more superficial layer of the dLGN receives projections from the ipsilateral eye, a unique situation among the members of the Order Primates. This observation adds support to the proposal that Tarsius does not share a more recent common ancestry with simians as compared with lemuriform and lorisiform primates.

Animals↗
PubMed1995

Nerve terminals of mucous gland electroreceptors in the platypus (Ornithorhynchus anatinus).

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.

Animals↗
PubMed1994

Genomic evolution. Flying DNA.

The extremely high AT content of bat DNA complicates the reconstruction of bat phylogeny from DNA sequence data, but may help throw light on genomic evolution.

Animals↗
PubMed1993

Retinotopic organization of the primary visual cortex of flying foxes (Pteropus poliocephalus and Pteropus scapulatus).

The representation of the visual field in the occipital cortex was studied by multiunit recordings in seven flying foxes (Pteropus spp.), anesthetized with thiopentone/N2O and immobilized with pancuronium bromide. On the basis of its visuotopic organization and architecture, the primary visual area (V1) was distinguished from neighboring areas. Area V1 occupies the dorsal surface of the occipital pole, as well as most of the tentorial surface of the cortex, the posterior third of the mesial surface of the brain, and the upper bank of the posterior portion of the splenial sulcus. In each hemisphere, it contains a precise, visuotopically organized representation of the entire extent of the contralateral visual hemifield. The representation of the vertical meridian, together with 8-15 degrees of ipsilateral hemifield, forms the anterior border of V1 with other visually responsive areas. The representation of the horizontal meridian runs anterolateral to posteromedial, dividing V1 so that the lower visual quadrant is represented medially, and the upper quadrant laterally. The total surface area of V1 is about 140 mm2 for P. poliocephalus, and 110 mm2 for P. scapulatus. The representation of the central visual field is greatly magnified relative to that of the periphery. The cortical magnification factor decreases with increasing eccentricity, following a negative power function. Conversely, receptive field sizes increase markedly with increasing eccentricity, and therefore the point-image size is approximately constant throughout V1. The emphasis in the representation of the area centralis in V1 is much larger than that expected on the basis of ganglion cell counts in flat-mounted retinas. Thus, a larger degree of convergence occurs at the peripheral representations in the retino-geniculo-cortical pathway, in comparison with the central representations. The marked emphasis in the representation of central vision, the wide extent of the binocular field of vision, and the relatively large surface area of V1 reflect the importance of vision in megachiropterans.

Animals↗
PubMed1992

Common principle of guidance by echolocation and vision.

1. Using echolocation, bats move as gracefully as birds through the cluttered environment, suggesting common principles of optic and acoustic guidance. We tested the idea by analysing braking control of bats (Macroderma gigas) flying through a narrow aperture with eyes covered and uncovered. 2. Though braking control would seem to require rapid detection of distance and velocity and computation of deceleration, simpler control is possible using the tau function of any sensory variable S that is a power function of distance to aperture. Tau function of S is tau (S) = S/S (the dot means time derivative). Controlled braking is achievable by keeping tau (S) constant. 3. Previous experiments indicated the tau (S) constant procedure is followed by humans and birds in visually controlling braking. Analysis of the bats' flight trajectories indicated they too followed the braking procedure using echolocation. 4. The tau function of echo-delay or of echo-intensity or of angle subtended by directions of echoes from two points on the approach surface could be used to control braking. Aperture size was modulated during flight on some trials in an attempt to test between these possibilities, but the results were inconclusive.

Animals↗
PubMed1992

Retinal topography in the koala (Phascolarctos cinereus).

Nissl-stained retinal wholemounts were used to investigate the topographical organization of the ganglion cell layer of the koala (Phascolarctos cinereus); the visual resolution limit of this animal was subsequently estimated from retinal ganglion cell density data. Two types of cells could be differentiated on the basis of their size and staining characteristics: a subpopulation of presumed ganglion cells, consisting of medium to large cells with Nissl substance in the cytoplasm and pale uniformly staining nuclei, and a further subpopulation of small, densely staining cells. The latter group were presumed to be neuroglia and displaced amacrine cells. Iso-density contour maps were prepared from total cell counts and also counts of presumed ganglion cells; in all cases, the density of cells was greatest in the inferior retina where there was an area of peak density occurring as a poorly developed, horizontal streak that extended across the inferior retina. The inferior position of the streak in the koala contrasts with reports of the superior position of streaks in other marsupials. Peak cell densities of 2370 cells/mm2 and 1480 cells/mm2 were recorded for the total cell population and the presumed ganglion cell subpopulation, respectively. The latter value is equivalent to a visual resolution of 2.4 cycles/degree, based on sampling theory and a square packing paradigm, placing the koala close in visual performance to two other marsupials, the Australian Northern native cat and the American Virginia opossum.

Animals↗
PubMed1992

The primary structure of the hemoglobin from the tomb bat (Taphozous georgianus, Microchiroptera).

The primary structures of the alpha- and beta-chains of the single hemoglobin component from the tomb bat (Taphozous georgianus, Microchiroptera) are presented. After chain separation by reversed-phase HPLC the sequences could be determined by automatic gas and liquid phase Edman degradation of the chains and their tryptic peptides. The alpha- and beta-chains differ from human hemoglobin by 14 and 18 replacements, respectively. Compared to the total number of amino-acid exchanges, the exchange rate in the interhelical regions of the alpha-chains is surprisingly high (25%). It seems unlikely that substitutions at contact positions affect the oxygen binding properties of the hemoglobin.

Amino Acid Sequence↗