Neuromuscular organization of avian flight muscle: Morphology and contractile properties of motor units in the pectoralis (pars thoracicus) of pigeon (Columba livia)

We used acid digestion and glycogen depletion to determine fascicle organization, fiber morphology, and physiological and anatomical features of individual motor units of an in-series muscle, the pectoralis (pars thoracicus) of the pigeon (Columba livia). Most fascicles are attached at one end to connective tissue. Average fiber length in the four regions examined range from 42% to 66% of average fascicle length. More than 65% of fibers are blunt at one end of a fascicle and taper intrafascicularly. Fibers with blunt–blunt endings range from 13% to 31% of the population in different regions; taper–taper fibers range from 2% to 17%. Pigeon pectoralis fibers are distinguished histochemically into fast-twitch glycolytic (FG) and fast-twitch oxidative-glycolytic (FOG) populations. Three units composed of FG fibers (FG units) contract more quickly than three units composed of FOG fibers (FOG units) (range 31–37 vs 47–62 msec), produce more tetanic force (0.11–0.32 vs 0.02–0.05 N) and are more fatigable (<18% initial force vs >50% after repeated stimulation). Most motor units are confined to one of the four muscle regions. Territory of two FOG units is <30% of parent fascicle length. Territories of other units spanned parent fascicles; most fibers in these units do not extend the full fascicle length. Compared to FG units, FOG units have lower maximum innervation ratios and density indices (ratio of depleted/total FOG fibers in territory 8–14% vs 58–76% for FG units). These differences support the hypothesis that FG units are organized to produce substantial force and power for takeoff, landing and other ballistic movements whereas FOG units are suited for sustained flight when power requirements are reduced. Implications of findings for understanding the control of in-series muscles and the use of connective tissue elastic elements during wing movements are discussed. J.Morphol. 236:179–208, 1998. © 1998 Wiley-Liss, Inc.     

The spectral sensitivity of single units in the nucleus rotundus of pigeon, Columba livia

Responses to diffuse monochromatic light were recorded from single units in the diencephalon of pigeon. Units were both excited and inhibited by light stimulation. Intensity-response functions based on latency measures to the first spike after stimulation were used to generate action spectra. One class of spectral sensitivity functions presumably from rods, showed peak sensitivities near 500 nm: these functions were unaffected by changing criterion values used to generate the functions. A second class of cone functions showed multiple peak sensitivities at 540 nm and 600–620 nm. These units shifted their peak sensitivities with a change in criterion values. Unit response types tended to be localized differentially in the nucleus rotundus. Excitatory units were located in the dorsal half of the nucleus, while inhibitory units were located in the ventral half, with a few exceptions. An attempt was made to integrate the present findings with previous behavioral, electrophysiological, photochemical, and anatomical data in the pigeon.     

Functional anatomy of the pigeon hand (Columba livia): A muscle stimulation study

The morphology and function of all muscles controlling the pigeon hand were analyzed. Muscle action was determined in situ by inducing contraction via silver wire electrodes in anesthetized birds. EMG electrodes were implanted in the test muscle and an adjacent muscle to monitor contraction and volume conduction respectively. Results indicate that pigeons have fine control of hand and digit movements. However, the directions of movement are restricted. Movements have been eliminated or severely limited in those directions that experience strong stress during flight. Such restrictions may reduce the amount of muscular activity required for stabilization of the hand and its components. Mobility is retained in directions not subject to large stresses and where movement is essential for the kinematics of flight to be executed properly. © 1995 Wiley-Liss, Inc.     

Drinking behavior and jaw muscle (EMG) activity in the pigeon (Columba livia)

The relation between jaw movements and jaw muscle activity was examined during two different types of drinking in pigeons: tip and rictus drinking. The amplitude and duration of jaw opening is greater for rictus than for tip drinking, but both types involve individual cycles of jaw-opening and closing movements, organized into bouts. Cycle duration increases gradually over the initial portion of the bout and is relatively constant thereafter.Each drinking cycle is composed of an initial rapid jaw-opening component, a sustained opening phase of variable duration and a closing movement. The initial and final phases are related, respectively, to activity in the upper beak levator (protractor) and the jaw closer (adductor, pterygoid) muscles. The amplitude and duration of the sustained phase are correlated with the magnitude and duration of activity in the lower jaw opener (depressor). The kinematic and electromyographic organization of jaw movements during drinking is discussed in relation to the morphology of the jaw apparatus and the functional requirements of the behavior.Abbreviations AMEM adductor mandibulae externus muscle - DM depressor mandibulae muscle - EMG electromyographic - PQP protractor quadrati et pterygoidei muscle - PTP pseudotemporalis profundus muscle - PVL/PVM pterygoideus ventralis muscle, pars lateralis and medialis     

Neuromuscular organization and regional EMG activity of the pectoralis in the pigeon

In order to improve our understanding of the neuromuscular control of the most massive avian flight muscle, we studied the innervation pattern of the pigeon pectoralis. Nine primary branches from the rostral trunk and nine to ten branches from the caudal trunk of the pectoral nerve were identified by microdissection in ten pigeons. The region of muscle that each branch innervates was delineated by nerve stimulation studies (ten pigeons) and six regions were confirmed by glycogen depletion (ten pigeons). In pigeons, branches from the rostral nerve innervate the anterior 3/5 of the sternobrachialis (SB) head of the pectoralis and branches from the caudal trunk innervate the posterior 1/2 of the SB and all of the throacobrachials (TB). In the SB, individual branches of the rostral pectoral nerve innervate wedge-shaped muscle regions (each approximately 1.3 cm wide), collectively forming a fan shaped arrangement along the sternal carina. Adjacent muscle regions partially overlap at their boundaries. Within the thoracobrachialis (TB) head of the pectrolis, muscle regions are wider. There is a region in mid-SB-where the innervation territories of the rostral and caudal nerves oferlap. Electromyographic (EMG) activity patterns were recorded within ten of the identified muscle regions during take-off, level flapping flight, and landing. Onset of EMG activity and EMG intensity within various muscle regions exhibits significant differences both within a wingbeat cycle and among different modes of flight. The innervation pattern of the pectoralis presents the anatomical substrate for neuromuscular compartmentalization and differential EMG activity within the pectoralis may reflect sensory-motor partitioning. The extent to which the neuromuscular compartmentalization of the pectoralis corresponds to its ability to produce an array of force vectors to the wing awaits further more detailed biomechanical studies. © 1993 Wiley-Liss, Inc.     

Characterization of baroreflex gain in the domestic pigeon (Columba livia)

Birds have a remarkable capacity to regulate circulation yet little is known about the avian baroreflex. Although both linear regression and curve-fitting techniques are frequently used to assess baroreflex function in mammals, only the former technique has been used in birds. We characterized baroreflex gain in domestic pigeons (Columba livia) and compared gain values derived from applying linear regression to ramp changes in mean arterial pressure (MAP) to values derived from fitting a four-parameter sigmoidal function to steady-state alterations in MAP. We found that, unlike mammals, pigeons do not display circadian patterns in MAP, HR or gain derived from bolus injections of vasoactive drugs. The pressor, but not depressor response, was attenuated by administration of the NMDA-antagonist ketamine, suggesting that central processing of the baroreflex may be similar in birds and mammals despite anatomical differences in arterial baroreceptive zones. Because graded infusions of vasoactive drugs could not consistently produce a plateau in the HR response, fitting data to a sigmoidal curve was difficult. Thus, we propose that variations of the Oxford method and linear regression analysis are superior method to assess baroreflex gain in pigeons than curve fitting.     

The directionality of the ear of the pigeon (Columba livia)

Summary The directionality of cochlear microphonic potentials in the azimuthal plane was investigated in the pigeon (Columba livia), using acoustic free-field stimulation (pure tones of 0.25–6 kHz).At high frequencies in the pigeon's hearing range (4–6 kHz), changing azimuth resulted in a maximum change of the cochlear microphonic amplitude by about 20 dB (SPL). The directionality decreased clearly with decreasing frequency.Acoustic blocking of the contralateral ear canal could reduce the directional sensitivity of the ipsilateral ear by maximally 8 dB. This indicates a significant sound transmission through the bird's interaural pathways. However, the magnitude of these effects compared to those obtained by sound diffraction (maximum > 15 dB) suggests that pressure gradients at the tympanic membrane are only of subordinate importance for the generation of directional cues.The comparison of interaural intensity differences with previous behavioral results confirms the hypothesis that interaural intensity difference is the primary directional cue of azimuthal sound localization in the high-frequency range (2–6 kHz).Abbreviations CM cochlear microphonic potential - IID interaural intensity difference - IID-MRA minimum resolvable angle calculated from interaural intensity difference - MRA minimum resolvable angle - OTD interaural ongoing time difference - RMS root mean square - SPL sound pressure level     

Genetic analyses of visual pigments of the pigeon (Columba livia)

We isolated five classes of retinal opsin genes rh1(Cl), rh2(Cl), sws1(Cl), sws2(Cl), and lws(Cl) from the pigeon; these encode RH1(Cl), RH2(Cl), SWS1(Cl), SWS2(Cl), and LWS(Cl) opsins, respectively. Upon binding to 11-cis-retinal, these opsins regenerate the corresponding photosensitive molecules, visual pigments. The absorbance spectra of visual pigments have a broad bell shape with the peak, being called lambdamax. Previously, the SWS1(Cl) opsin cDNA was isolated from the pigeon retinal RNA, expressed in cultured COS1 cells, reconstituted with 11-cis-retinal, and the lambdamax of the resulting SWS1(Cl) pigment was shown to be 393 nm. In this article, using the same methods, the lambdamax values of RH1(Cl), RH2(Cl), SWS2(Cl), and LWS(Cl) pigments were determined to be 502, 503, 448, and 559 nm, respectively. The pigeon is also known for its UV vision, detecting light at 320-380 nm. Being the only pigments that absorb light below 400 nm, the SWS1(Cl) pigments must mediate its UV vision. We also determined that a nonretinal P(Cl) pigment in the pineal gland of the pigeon has a lambdamax value at 481 nm.     

Jaw movement kinematics and jaw muscle (EMG) activity during drinking in the pigeon (Columba livia)

Summary Movements of the maxilla and mandible were recorded during drinking in the head-fixed pigeon and correlated with electromyographic activity in representative jaw muscle groups. During drinking, each jaw exhibits opening and closing movements along both the dorso-ventral and rostro-caudal axes which may be linked with or independent of each other. All subjects showed small but systematic increases in cycle duration over the course of individual drinking bouts. Cyclic jaw movements during drinking were correlated with nearly synchronous activity in the protractor (levator) of the upper jaw and in several jaw closer muscles, as well as with alternating activity in tongue protractor and retractor muscles. No EMG activity was ever recorded in the lower jaw opener muscle, suggesting that lower jaw opening in this preparation is produced, indirectly, by the contraction of other muscles. The results clarify the contribution of the individual jaws to the generation of gape variations during drinking in this species.Abbreviations AMEM adductor mandibulae externus muscle - DM depressor mandibulae muscle - EMG electromyographic - GENIO geniohyoideus muscle - LB lower beak - LED light-emitting diode - PQP protractor quadrati et pterygoidei muscle - PVL pterygoideus ventralis muscle, pars lateralis - SeH/StH serpihyoideus or stylohyoideus muscle - UB upper beak     

Accumulation of calcium and phosphorus in pigeon (Columba livia) embryos

Summary Calcium and phosphorus were measured in the yolk and albumen of fertile pigeon (Columba livia) eggs incubated for 0–17 days, and in embryos and hatchlings. Shell provided most of the calcium for skeletal mineralization of the embryos, whereas phosphorus was derived from the yolk and albumen. Mobilization of calcium from the shell to the embryo commenced at approximately day 11 of incubation, accumulating both in the embryo and the yolk sac. There was 1.4 times more calcium in squab yolk sacs than that contained in newly laid egg yolks. The results suggest that whereas general patterns of calcium and phosphorus accumulation during embryogenesis in altricial birds closely resemble those of precocial birds, calcium mobilization from the shell begins later, proceeds at a slower rate and results in a less mineralized hatchling.CIDA/NSERC Visiting Research Associate Permanent address: Department of Animal Science, University of Peradeniya, Peradeniya, Sri Lanka     

Morphologic study of the efferent ductules of the pigeon (Columba livia)

The efferent ductules of the pigeon are localized in the epididymal region and are topographically divided into proximal and distal, both portions being lined with stereociliated pseudostratified epithelium. Transmission electron microscopy shows five distinct cell types: light, dark, and angular non-ciliated cells with possible apocrine secretory role cells and halo cells, possibly intraepithelial leucocytes. The proximal efferent ductules have the widest diameter among all ductules in the epididymal region.     

A behavioral study of vibrational sensitivity in the pigeon (Columba livia)

Summary The pigeon (Columba livia) has a well-developed ability to detect weak vibrations. Using the method of heart-rate conditioning the vibrational sensitivity was determined for four pigeons at an error probability of P<0.025. The threshold-frequency relationships indicate that the greatest sensitivity to vibrational stimuli is found in the frequency range from 300 to 1,000 Hz with thresholds of about 0.1 m; lowest threshold is 0.04 m at 500 Hz (Fig. 4). Pigeons can respond not only to the frequency of a stimulus, but also to its intensity. The interval decrement (in %) of ECG is a positive correlative function of the stimulus intensity, the calculated values being approximately 4–5% per order of magnitude of the stimulus amplitude (in m) at best frequencies (Fig. 5). The value of vibration detection for birds is discussed.Abbreviation ECG electrocardiogram     

Jaw muscle (EMG) activity and amplitude scaling of jaw movements during eating in pigeon (Columba livia)

During each phase of the pigeon's eating sequence, jaw opening amplitude (gape) is adjusted to the size of the food object; first prior to contact (Grasping), again in positioning the food (Stationing), and finally, during its movement through the oral cavity (Intraoral Transport). Part I of this study examined jaw movement kinematics during ingestion of different size food pellets to determine the relative contribution of velocity and rise time variables. Part II specified the muscle activity patterns mediating each phase of the eating sequence, and determined how these patterns are modulated to produce adjustments of gape size.The relative contribution of velocity and rise time variables to the control of gape differs in each phase of the eating sequence. However, for any pellet size, variations in opening rise time may function in a compensatory manner to minimize gape undershooting. Each phase of the eating sequence is mediated by a characteristic muscle activity pattern. The adjustment of gape size to pellet size involves systematic modulation of this pattern, and the parameters modulated differ in the different phases in a manner which may reflect the functional requirements of each phase.Abbreviations AMEM adductor mandibulae externus muscle - DM depressor mandibulae muscle - EMG electromyographic - PDC/PDR pterygoideus muscle, pars dorsalis caudalis and rostralis - PQP protractor quadrati et pterygoidei muscle - PTP pseudotemporalis profundus muscle - PVL/PVM pterygoideus ventralis muscle, pars lateralis and medialis     

Cooling by cutaneous water evaporation in the heat-acclimated rock pigeon (Columba livia)

The present study provides an up-to-date overview of the cutaneous water-evaporation cooling mechanism in the rock pigeon. Cutaneous water evaporation fully replaces the classic respiratory cooling mechanism in the resting, heat-acclimated bird, and is more economical in terms of water conservation. It enables the pigeon to maintain homeostasis, and to breed successfully in harsh environments. Adrenergic signaling is involved in the initiation of this novel mechanism, either by deactivation of the beta-adrenergic receptors (ARs), or activation of the alpha-AR. The adrenergic signaling results in a marked increase in cutaneous blood flow and in the arterial-to-venous blood-flow ratio. This is associated with alterations in the cutaneous capillary wall ultrastructure, which increase its permeability to plasma proteins and water. The end result of this process might be an increase in water efflux from the capillary lumen. The properties of beta-ARs were measured in the cardiac muscle of thermal-acclimated pigeons. Significant down-regulation in the density of beta-ARs, associated with increased affinity of these receptors, was measured in the heat-acclimated pigeon. Concomitantly, changes in the skin ultrastructure and lipid composition were found in very well defined patches in the epidermis of heat-acclimated pigeons. These suppress the skin resistance to water transfer. We suggest that this cooling mechanism involves finely orchestrated adjustments in the ultrastructure of the skin and the cutaneous capillaries, and in skin blood flow. Adrenergic signals are among those factors that regulate this cooling mechanism during exposure to a hot environment.     

Circadian organization in the pigeon,Columba livia: the role of the pineal organ and the eye

Summary The roles of the pineal organ and the eye in the control of circadian locomotor rhythmicity were studied in the pigeon (Columba livia). Neither pinealectomy nor blinding abolished the circadian rhythms in constant dim light conditions (LLdim). All the pinealectomized birds and the blinded birds entrained to light-dark (LD) cycles with no discernible anticipatory activity. However, the birds which had been both pinealectomized and blinded showed no circadian rhythms in prolonged LLdim. These birds entrained to LD cycles with anticipatory activity and showed residual rhythmicity for a while after transfer from LD cycles to LLdim. Continuous administration of melatonin induced suppression of the circadian rhythms and reduced total amount of locomotor activity in LLdim. These results suggest that not only the pineal organ but also the eye (perhaps the retina) is involved in the pigeon's circadian system.Abbreviations NAT N-acetyltransferase - LLdim constant dim light - cadian period - SCN suprachiasmatic nucleus - circadian activity time - LD light-dark     

Vascular reactivity of the brain in the pigeon Columba livia

In experiments on awake relatively unrestrained pigeons, studies have been made on the reactions of the cerebrovascular bed to fixed functional loads of physical (orthostasis) and chemical (inhalation of hypoxic and hypercapnic gas mixtures) nature. Using hydrogen clearance method, the increase in the intensity of local cerebral blood flow in different structures of the telencephalon during inhalation of the mentioned gas mixtures was demonstrated. Bilateral vagotomy resulted in inversed reactions. Influence of functional loads was accompanied by changes in rheoencephalographic parameters. The data obtained suggest the existence of an evident reactivity of cerebral vessels in birds which is controlled by neurogenic mechanism of regulation of vascular tone.