Specializations in the lumbosacral spinal cord of birds: morphological and behavioural evidence for a sense of equilibrium.

Birds have a variety of long known anatomical specializations both in the vertebrae and in the spinal cord of lumbosacral segments. In the present investigation additional morphological specializations are described for the pigeon. These consist of segmentally organized semicircular canal-like structures (lumbosacral canals) which together with specializations in the meninges of the spinal cord form a large liquor space above accessory lobes attached to the spinal cord. The whole system is thought to function as a sense of equilibrium. The neurons in the lobes are assumed to be sensory neurons which are stimulated by the inertia of the fluid during movements of the body. Such a function is supported by lesion experiments: opening of the fluid space was followed by severe disturbances of landing and walking behavior.     

Behavioral evidence of the role of lumbosacral anatomical specializations in pigeons in maintaining balance during terrestrial locomotion

In birds there are anatomical specializations in the lumbosacral vertebrae and spinal cord. These include segmentally organized bony canals which are related to accessory lobes of the spinal cord. Both structures are connected by cerebrospinal fluid. To test whether these specializations function as a sense organ of equilibrium the effect of opening the fluid space was studied in pigeons. Locomotory behaviors on the ground (landing on a perch, keeping balance on a rotating perch, walking) but not flight were significantly impaired after lesion. These results support the assumption that the lumbosacral specializations are involved in the control of locomotion on the ground. Accepted: 12 March 2000     

The tarso-pretarsal chordotonal organ as an element in cockroach walking

Many types of sense organs have been demonstrated to show repetitive discharges during walking that could provide informational cues about leg movements and other parameters of locomotion. We have recorded activities of receptors of the distal (tarsal) segments of the cockroach hindleg in restrained and freely moving animals while they were videotaped. These recordings show peaks of activities at the onset and termination of the stance phase. We have morphologically and physiologically identified a joint angle receptor, the tarso-pretarsal chordotonal organ, that contributes to the discharges seen late in stance, prior to the onset of leg flexion in swing. This sense organ encodes the angle and rate of change of the most distal leg joint and specifically discharges when the claws are disengaged from the substrate. Applied displacements of the claws in restrained preparations elicit reflex activation of the tibial flexor muscle and a crossed extensor reflex in the opposite hindleg. These reflexes could function to insure that leg flexion in swing does not occur until the claws are disengaged and to enhance support by the opposite hindleg. Thus, the regular discharges of the chordotonal organ could assure efficient and coordinated muscle contractions and movements during normal, unperturbed walking. Accepted: 2 January 1997     

鸟类的发声系统和调控机制

鸟类是具有复杂声行为的动物,其拥有特殊的发声器官——鸣管。尽管鸣禽与非鸣禽的发声特性和发声器官解剖学差异较大,但是两者发声运动控制模式相似。文章综述了近年来鸟类呜声研究的新进展,重点比较了呜禽和非鸣禽发声器官的结构功能特点和发声特性调控的异同。作为一种动物模型,鸟类发声系统能为人类语言学习等研究提供借鉴。     

Intracellular recording from a spider vibration receptor

The present study introduces a new preparation of a spider vibration receptor that allows intracellular recording of responses to natural mechanical or electrical stimulation of the associated mechanoreceptor cells. The spider vibration receptor is a lyriform slit sense organ made up of 21 cuticular slits located on the distal end of the metatarsus of each walking leg. The organ is stimulated when the tarsus receives substrate vibrations, which it transmits to the organ’s cuticular structures, reducing the displacement to about one tenth due to geometrical reasons. Current clamp recording was used to record action potentials generated by electrical or mechanical stimuli. Square pulse stimulation identified two groups of sensory cells, the first being single-spike cells which generated only one or two action potentials and the second being multi-spike cells which produced bursts of action potentials. When the more natural mechanical sinusoidal stimulation was applied, differences in adaptation rate between the two cell types remained. In agreement with prior extracellular recordings, both cell types showed a decrease in the threshold tarsus deflection with increasing stimulus frequency. Off-responses to mechanical stimuli have also been seen in the metatarsal organ for the first time.     

A comparison of the oxygen consumption/body weight relationship obtained during submaximal exercise on a bicycle ergometer and on a treadmill.

It is widely accepted that the relationship between oxygen consumption and body weight obtained during exercise on a bicycle ergometer differs from that obtained during treadmill walking. Experimental evidence to support this claim is lacking. To examine this difference a group of subjects (body weight 41--81 kg) undertook a predetermined level of submaximal exercise on a bicycle ergometer and a treadmill. Oxygen consumption was measured in a steady state at rest (i.e. sitting on the bicycle ergometer and standing on the treadmill) and during the two modes of exercise. A significant positive correlation between oxygen consumption and body weight was obtained under all four conditions of measurement. At rest the two regression lines did not differ in slope or elevation. During exercise the slope and the elevation of the line obtain from treadmill walking were significantly greater than from bicycle ergometer exercise. The 'metabolic cost' of bicycle ergometer exercise, (Vo2 during exercise--V02 at rest), showed no significant correlation with body weight. In contrast, there was a significant positive correlation during walking. It is suggested that these differences have arisen due to a different proportion of the total body weight supported by the subject in the two forms of exercise.     

Light- and electron-microscopic analysis of a complex sensory organ: The tegula of Locusta migratoria

Summary Structure and organization of the tegula, a cupola-shaped structure located at the anterior base of the wings of locusts, is described using various morphological methods. Based on histological and cytological criteria, two different sensory systems are distinguished: (1) a field of mechanoreceptive hairs, and (2) a chordotonal organ. The total number of sensory cells corresponds to the number of axons within the nerve supporting the tegula. The hairs are situated at the posterior region of the tegula, and each hair is innervated by only one sensory cell. The complex architecture of the chordotonal organ is analyzed and the attachment of the scolopidia to the cuticle is described. A single scolopidium makes contact with several epidermal cells. The attachment cells run in parallel and are oriented longitudinally within the tegula, being connected to each other and to the epidermal cells by desmosomes. A function in relation to wing movements during flight is suggested for the two sensory systems within the mixed sense organ, tegula.     

Neither season nor sex affects the cost of terrestrial locomotion in a circumpolar diving duck: the common eider (Somateria mollissima)

Locomotion accounts for a significant proportion of the energy budget in birds, and selection is likely to act on its economy, particularly where energy conservation is essential for survival. Birds are capable of different forms of locomotion, such as walking/running, swimming, diving and flying, and adaptations for these affect the energetic cost [cost of locomotion (CoL)] and kinematics of terrestrial locomotion. Furthermore, seasonal changes in climate and photoperiod elicit physiological and behavioural adaptations for survival and reproduction, which also influence energy budget. However, little is understood about how this might affect the CoL. Birds are also known to exhibit sex differences in size, behaviour and physiology; however, sex differences in terrestrial locomotion have only been studied in two cursorially adapted galliform species in which males achieved higher maximum speeds, and in one case had a lower mass-specific CoL than females. Here, using respirometry and high-speed video recordings, we sought to determine whether season and sex would affect the CoL and kinematics of a principally aquatic diving bird: the circumpolar common eider (Somateria mollissima). We demonstrate that eiders are only capable of a walking gait and exhibit no seasonal or sex differences in mass-specific CoL or maximum speed. Despite sharing identical limb morphometrics, the birds exhibited subtle sex differences in kinematic parameters linked to the greater body mass of the males. We suggest that their principally aquatic lifestyle accounts for the observed patterns in their locomotor performance. Furthermore, sex differences in the CoL may only be found in birds in which terrestrial locomotion directly influences male reproductive success.     

Activity and functions of the human gluteal muscles in walking,running, sprinting,and climbing

It has been suggested that the uniquely large gluteus maximus (GMAX) muscles were an important adaptation during hominin evolution based on numerous anatomical differences between humans and extant apes. GMAX electromyographic (EMG) signals have been quantified for numerous individual movements, but not across the range of locomotor gaits and speeds for the same subjects. Thus, comparing relative EMG amplitudes between these activities has not been possible. We assessed the EMG activity of the gluteal muscles during walking, running, sprinting, and climbing. To gain further insight into the function of the gluteal muscles during locomotion, we measured muscle activity during walking and running with external devices that increased or decreased the need to control either forward or backward trunk pitch. We hypothesized that 1) GMAX EMG activity would be greatest during sprinting and climbing and 2) GMAX EMG activity would be modulated in response to altered forward trunk pitch demands during running. We found that GMAX activity in running was greater than walking and similar to climbing. However, the activity during sprinting was much greater than during running. Further, only the inferior portion of the GMAX had a significant change with altered trunk pitch demands, suggesting that the hip extensors have a limited contribution to the control of trunk pitch movements during running. Overall, our data suggest that the large size of the GMAX reflects its multifaceted role during rapid and powerful movements rather than as a specific adaptation for a single submaximal task such as endurance running. Am J Phys Anthropol 153:124–131, 2014. © 2013 Wiley Periodicals, Inc.     

The Ultrastructure of the Accessory Olfactory Organ in the River Lamprey (Lampetra Jiuviatilis)

The accessory olfactory organ of Lampetra fluviatilis was found to consist of clusters of interconnected vesicles in tenuous connection with the exterior medium via the cavity of the olfactory organ. The walls of the vesicles are composed of two types of cells. One type are primary sense cells that resemble the olfactory sense cells in that their nucleus is situated peripherally and their axons pass directly into the brain. They differ from the olfactory sense cells in the size and number of cilia they bear, and also in the internal structure of the cilia. The second cell type are supporting and/or secretory cells. It is concluded that this sense organ is capable of responding to a “special kind” of chemical stimulus and its possible function is discussed.     

Evolutionary changes in sensory precursor formation in arthropods: embryonic development of leg sensilla in the spider Cupiennius salei

We describe here for the first time the development of mechanosensory organs in a chelicerate, the spider Cupiennius salei. It has been shown previously that the number of external sense organs increases with each moult. While stage 1 larvae do not have any external sensory structures, stage 2 larvae show a stereotyped pattern of touch sensitive ‘tactile hairs’ on their legs. We show that these mechanosensory organs develop during embryogenesis. In contrast to insects, groups of sensory precursors are recruited from the leg epithelium, rather than single sensory organ progenitors. The groups increase by proliferation, and neural cells delaminate from the cluster, which migrate away to occupy a position proximal to the accessory cells of the sense organ. In addition, we describe the development of putative internal sense organs, which do not differentiate until larval stage 2. We show by RNA interference that, similar to Drosophila, proneural genes are responsible for the formation and subtype identity of sensory organs. Furthermore, we demonstrate an additional function for proneural genes in the coordinated invagination and migration of neural cells during sensory organ formation in the spider.     

A new cephalic type of presumed sense organ with naked dendritic ends in the atypical male of the parasitic copepod Pachypygus gibber (Crustacea)

Summary The topography, external structure and ultrastructure of a cephalic sense organ, described for the first time, were studied by light and electron microscopy in the parasitic copepod Pachypygus gibber. This species is unusual in that it has three reproductive sexual forms (two males, one female).The cephalic organ, present only in the atypical male, is made up of numerous functional units, each composed of 4 cells: two sensory cells, one basal enveloping cell and one apical canal-forming cell opening outside via a pore. Many hundred pores are situated within the cuticle of the ventral pleural borders. Through each pore protrude two ciliary endings.An interesting feature is that the ciliary ends are without cuticular cover and thus, directly exposed to the surroundings, a situation unique in arthropods.The structural characteristics of this sense organ and the particular mode of life of the atypical male (with an additional free planktonic phase), lead to the hypothesis that its function is linked to chemical reception in the complex behavioural patterns such as host and sex recognition, during the free life.     

Ultrastructure of the antennal sensilla of aphids

Summary An electron microscopical study of aphid antennal sensilla has revealed two types of trichoid sensilla. Type I, innervated by a single neuron is mechanoreceptive; type II, innervated by three to five neurons is both mechanoreceptive and chemoreceptive with possibly a third function. Johnston's organ in the pedicel comprises a peripheral ring of scolopidia inserted into the joint with the flagellum; two non-peripheral groups of scolopidia lie in the lumen with attachment points in the wall of the third segment. The fine structure of a campaniform sensillum on the pedicel is described together with two homologous and previously unknown sense organs at the joint between the fifth and sixth antennal segments. An unusually placed scolopidium in the lumen of the sixth segment has also been found. The function of this scolopidium is unknown but Johnston's organ, the campaniform sensillum and joint receptors are suggested to act as antennal proprioceptors.The authors thank the Long Ashton Research Station, Bristol for use of the SEM facilities. A.K. Bromley gratefully acknowledges the tenure of a S.R.C. CASE Studentship and thanks Professor L.H. Finlayson for research facilities     

Glutamate evokes firing through activation of kainate receptors in chick accessory lobe neurons

Ten pairs of protrusions, called accessory lobes (ALs), exist at the lateral sides of avian lumbosacral spinal cords. Histological and behavioral evidence suggests that neurons are present in ALs and the AL acts as a sensory organ of equilibrium during walking. Neurons in the outer layer of the AL consistently show glutamate-like immunoreactivity and neurons in the central region of the AL show glutamate receptor-like immunoreactivity. However, it is unknown how glutamate acts on the functional activity of AL neurons. In this study, we examined the effects of glutamate on the electrical activities of AL neurons using the patch clamp technique. There are two types of neurons among isolated AL neurons: spontaneously firing and silent neurons. Among silent neurons, 42 % of neurons responded to glutamate and generated repetitive firing. Kainate and glutamate in combination with the NMDA receptor antagonist, MK-801, also induced firing and evoked an inward current. On the other hand, the application of AMPA, NMDA or glutamate in combination with the non-NMDA receptor antagonist, CNQX, did not. These results indicate that chick AL neurons express functional kainate receptors to respond to glutamate and suggest that the glutamatergic transmission plays a role in excitatory regulation of AL neurons of the chick.     

Speed adaptation in a powered transtibial prosthesis controlled with a neuromuscular model

Control schemes for powered ankle-foot prostheses would benefit greatly from a means to make them inherently adaptive to different walking speeds. Towards this goal, one may attempt to emulate the intact human ankle, as it is capable of seamless adaptation. Human locomotion is governed by the interplay among legged dynamics, morphology and neural control including spinal reflexes. It has been suggested that reflexes contribute to the changes in ankle joint dynamics that correspond to walking at different speeds. Here, we use a data-driven muscle-tendon model that produces estimates of the activation, force, length and velocity of the major muscles spanning the ankle to derive local feedback loops that may be critical in the control of those muscles during walking. This purely reflexive approach ignores sources of non-reflexive neural drive and does not necessarily reflect the biological control scheme, yet can still closely reproduce the muscle dynamics estimated from biological data. The resulting neuromuscular model was applied to control a powered ankle-foot prosthesis and tested by an amputee walking at three speeds. The controller produced speed-adaptive behaviour; net ankle work increased with walking speed, highlighting the benefits of applying neuromuscular principles in the control of adaptive prosthetic limbs.     

Voltage-gated Ca2+ channels in accessory lobe neurons of the chick

Birds have ten pairs of protrusions, “accessory lobes”, on the lateral sides of the lumbosacral spinal cord. It has been proposed that accessory lobes act as a sensory organ of equilibrium and neurons in accessory lobes transmit sensory information to the motor center. We have reported that cells in chick accessory lobes express functional voltage-gated Na⁺ and K⁺ channels and generate action potentials. In this study, we examined properties of voltage-gated Ca²⁺ channels (VGCCs). The amplitude of voltage-gated Ca²⁺ channel currents carried by Ca²⁺ and Ba²⁺ increased gradually during 10 min rather than showing the usual run-down. The current–voltage relationship of Ba²⁺ currents was consistent with that of the high-voltage-activated Ca²⁺ channel. The proportion of Ba²⁺ currents inhibited by ω-conotoxin GVIA was larger than 80 %, indicating that the major subtype is N type. Amplitudes of tail currents of Ca²⁺ currents evoked by repetitive pulses at 50 Hz are stable for 1 s. If the major subtype of VGCCs at synaptic terminals is also N type, this property may contribute to the establishment of stable synaptic connections between accessory lobe neurons, which are reported to fire at frequencies higher than 15 Hz, and postsynaptic neurons in the spinal cord.     

Sense organs in Pycnogonida: A review

The Pycnogonida or sea spiders are exclusively marine invertebrates, numbering about 1,300 described species worldwide. Given their remarkable position in phylogeny as basal chelicerates or even basal euarthropods, the structure of their sense organs can reveal important characters, which—in a comparative framework—provide arguments to phylogenetic discussions and help to develop scenarios of evolutionary transformations. This review summarizes current knowledge and presents new original data on the sense organs in pycnogonids, that is, the eyes, the lateral sense organs and the ciliary or sensillar sense organs. Except for the eyes, there are not many detailed studies available. The ultrastructure of the R‐cells of the four eyes located on the ocular tubercle is described as “pseudoinverted”. The eyes are innervated to two visual neuropils located in the protocerebrum. The features of the lateral sense organ, also located on the ocular tubercle, are hitherto not conclusively resolved, a chemo‐ or thermoreceptive function is suggested. Finally, an overview of the various ciliary or sensillar sense organs distributed all over the body is given and the fine structure of branched setae is shown for the first time. The morphology of the sense organs of pycnogonids is compared with that of other arthropod taxa and assessed against the background of current theories of arthropod evolution.     

Development of leg chordotonal sensory organs in normal and heat shocked embryos of the cricket Teleogryllus commodus (Walker)

This paper describes the embryonic development of some parts of the sensory peripheral nervous system in the leg anlagen of the cricket Teleogryllus commodus in normal and heat shocked embryos. The first peripheral neurons appear at the 30% stage of embryogenesis. These tibial pioneer neurons grow on a stereotyped path to the central nervous system and form a nerve which is joined by the growth cones of axons that arise later, including those from the femoral chordotonal organ, subgenual organ and tympanal organ. The development of these organs is described with respect to the increase in number of sensory receptor cells and the shape and position of the organs. At the 100% stage of embryogenesis all three organs have completed their development in terms of the number of sense cells and have achieved an adult shape. To study the function of the tibial pioneer neurons during embryogenesis a heat shock was used to prevent their development. Absence of these neurons has no effect on the development of other neurons and organs proximal to them. However, the development of distal neurons and organs guided by them is impaired. The tibial pioneer neurons grow across the segmental boundary between femur and tibia early in development, and the path they form seems to be essential for establishing the correct connections of the distal sense organs with the central nervous system.     

The osteocyte as a wiring transmission system

The mechanism of transduction of mechanical strains into biological signals remains one of the more baffling problems of skeletal homeostasis. The updated literature ascribes to osteocytes the function of sensing the strains induced into the bone matrix by mechanical stresses. Whether the osteocytes perform such function by themselves or they are helped by other cells is also unknown. Indeed TEM investigations carried out in our laboratory pointed out the existence of a functional syncytium among all the cells of the osteogenic lineage (COL; stromal cells, osteoblasts or bone lining cells, osteocytes). On the basis of this finding, we suggested that COL may reciprocally modulate their function not only by volume transmission (paracrine and autocrine stimulation) but also by wiring transmission, namely in a neuronal like manner. Thanks to their location, osteocytes should theoretically be the first cells of COL functional syncytium to sense mechanical strains, whereas stromal cells should be the first to be activated by hormonal molecules diffusing across the endothelial lining. Since PTH and Estrogen receptors have also been localized on osteocytes, and considering that such hormones have been suggested to modulate the sensitivity to strain of the bone mechanosensor, we suggested that the osteocyte syncytium may constitute the microscopic bone structure that sense both mechanical strain and biochemical factors and, at any moment, after having combined the two types of stimuli, issues the appropriate signals to the other bone cells by volume and/or wiring-transmission. Stromal cells, on the other hand, besides transmitting signals from vascular endothelium to bone cells, may control the differentiation and then direct the course of the osteoblasts around the vascular framework.