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Biomedical subjects

O W Henson

Publications and source records attributed to O W Henson.

At least 19 recordsLinked to original sources

Morphology of the abdominal wall in the bat, Pteronotus parnellii (Microchiroptera: Mormoopidae): implications for biosonar vocalization.

We investigated the structure of the abdominal wall of Pteronotus parnellii and made comparisons with eight other species of Microchiroptera and one megachiropteran. Similar to other mammals, the abdominal wall of bats consists of the three flank muscles laterally and the m. rectus abdominis ventrally. In Microchiroptera, flank muscles are mostly confined to dorsal portions of the wall. The mm. transversus abdominis and obliquus internus abdominis form the bulk of the wall; the m. obliquus externus is poorly developed. Ventrolaterally, a large portion of the wall is a dense, bilaminar aponeurosis, composed of collagen, elastin, and fibroblasts. The thicker, superficial lamina derives from the mm. obliquus internus and transversus abdominis. The deep lamina is a continuation of the transversalis fascia. Collagen fibers of the two fused laminae are oriented orthogonally, resulting in a resilient, composite fabric. Fascicles of the flank muscles are oriented along the margins of the aponeurosis so that their forces appear to be concentrated onto the aponeurosis. We suggest that this system is adapted for the regulation and generation of intra-abdominal pressure. The abdominal wall of Pteropus, the one megachiropteran examined, lacks the derived aponeurosis and is similar to other mammals. We consider the abdominal wall of Microchiroptera to be analogous to the diaphragma, in that it functions in the regulation of pressure within body cavities and facilitates biosonar vocalization.

Abdominal Muscles

The effect of contralateral stimulation on cochlear resonance and damping in the mustached bat: the role of the medial efferent system.

In the unanesthetized mustached bat, stimulation of the ear with an acoustic transient produces damped oscillations which are evident in the cochlear microphonic potential. In this report we demonstrate how the decay time of these oscillations is affected by broadband noise presented to the contralateral ear (CLN). In the absence of CLN, the mean decay time was 1.94 +/- 0.23 ms, but during the presentation of CLN the decay time consistently decreased. The changes were finely graded, the higher the CLN, the greater the change. The effect could be maintained at a constant level for extended periods of time and this was evident when the CLN exceeded 40 dB SPL. The latency of the reflex for 64 dB noise was about 11 ms and near maximum changes occurred within 15 ms of CLN onset. Sectioning medial efferent nerve fibers in the floor of the fourth ventricle or the administration of a single dose of gentamicin eliminated changes produced by CLN. The prominence of CM responses to damped oscillations and the robust changes in response to CLN make the mustached bat an excellent model for studying the influence of the medial efferent system on cochlear mechanics.

Acoustic Stimulation

Detection and quantification of endolymphatic hydrops in the guinea pig cochlea by magnetic resonance microscopy.

Three-dimensional magnetic resonance microscopy (MRM) was used to study normal and hydropic cochleae of the guinea pig. With this technique consecutive serial slices representing the entire volume of isolated, fixed cochleae were obtained. The voxels (volume elements) making up the contiguous slices were isotropic (25 microns 3) and in each slice the boundaries of scala media, including the position of Reissner's membrane, were clearly delineated. Three-dimensional reconstructions of the endolymphatic and perilymphatic scale were generated. Custom software was developed to quantify cross-sectional area (CSA) of all scalae. In the normal cochlea all 3 scalae, including scala media, showed a gradual decrease in CSA from base to apex. Marked differences existed between our findings and previously reported cochlear dimensions, especially for the perilymphatic scalae in the basal turn. In hydropic cochleae the scala media was enlarged to a varying extent in different turns and marked changes in the degree of distension of Reissner's membrane occurred along the cochlea. MRM and subsequent computer analysis of the isotropic data provide excellent methods for imaging and quantifying the fluid spaces of normal and hydropic cochleae.

Animals

Respiratory muscle activity in relation to vocalization in flying bats.

The structure of the thoracic and abdominal walls of Pteronotus parnellii (Microchiroptera: Mormoopidae) was described with respect to their function in respiration and vocalization. We monitored electromyographic activity of respiratory and flight muscles in relation to echolocative vocalization. In flight, signals were telemetered with a small FM transmitter modified to summate the low-frequency myopotentials with biosonar signals from a ceramic-crystal microphone. Recordings were also made from the same bats confined to a small cage. Vocalizations were used as the parameter by which all muscle activities were correlated. A discrete burst of activity in the lateral abdominal wall muscles accompanied each vocalization. Diaphragmatic myopotentials occurred between groups of calls and did not coincide with activity of the abdominal wall or with vocalizations. Flight muscles were not active in resting bats. During flight, vocalizations and the abdominal muscle activity that accompanied them coincided with myopotentials of the pectoralis and serratus ventralis muscles. We propose that contractions of the lateral abdominal wall provide the primary power for the production of intense biosonar vocalization in flying and in stationary bats. In flight, synchronization of vocalization with activity of the pectoralis and serratus ventralis jointly contribute to the pressurization of the thoraco-abdominal cavity. This utilization of pressure that is normally generated in flight facilitates respiration and allows for the production of intense vocalizations with little additional energetic expenditure.

Abdominal Muscles

Brain activity patterns in flying, echolocating bats (Pteronotus parnellii): assessment by high resolution autoradiographic imaging with [3H]2-deoxyglucose.

Brain activity patterns during echolocation and flight were assessed in mustached bats (Pteronotus parnellii parnellii). Bats were injected intraperitoneally with [3H]2-deoxyglucose and restrained in a foam holder or allowed to fly for 20 min. Under resting conditions, low levels of [3H]2-deoxyglucose uptake were observed throughout the forebrain but relatively high uptake was found in brainstem auditory and vestibular centers. In flying, echolocating bats, marked increases in regional [3H]2-deoxyglucose uptake were apparent. All structures of the classical ascending auditory pathway were intensely labeled in autoradiograms. Other brain regions that exhibited high [3H]2-deoxyglucose uptake in flying bats included the cingulate cortex, stratum lacunosum-moleculare of the hippocampus, thalamus, caudate-putamen, superior colliculus, pontine reticular formation, nucleus ambiguus, parts of the midbrain central gray, and cerebellum. In the cerebellum, the most prominent increase in [3H]2-deoxyglucose uptake was found in discrete patches of the granule cell layer. The results provide the first overview of brain activity patterns during echolocation and flight in bats. In addition, uptake of [14C]fluorodeoxyglucose was used to compare brain activity patterns in flying bats to bats that were imaging their environment via biosonar while hanging in a wire cage. The echolocating-not-flying bats emitted 6931 +/- 1226 pulses in 20 min compared to 8972 +/- 1273 pulses in 20 min for flying bats. The uptake of the metabolic marker was significantly more in the flying bats compared to the emitting-not-flying bats in the medial geniculate, superior colliculus, auditory cortex, cingulate cortex and thalamus. In the nucleus ambiguus, cochlear nucleus, and inferior colliculus, uptake was similar for the flying and emitting-not-flying bats. These results suggest that the high metabolic activity observed in forebrain auditory regions of flying bats is related in part to neural processes that involve sensory motor integration during flight and not simply the perception of acoustic information.

Animals

AChE-staining of type II ganglion cells, processes and terminals in the cochlea of the mustached bat.

There have been a number of reports showing that ganglion cells of sensory neurons may be stained by traditional acetylcholinesterase (AChE) histochemical techniques commonly used to demonstrate efferent nerve fibers and terminals. AChE-staining has been described for cell bodies in the vestibular and spiral ganglia; staining of peripheral and central processes, however, is rare and the presence of reaction product in afferent terminals has not been reported. The outer hair cells of mustached bats, Pteronotus parnellii, differ from those of most mammals in that they typically have a single, large efferent terminal surrounded by 5-7 small, afferent terminals. In this animal an AChE-positive reaction was found not only in efferent fibers and terminals but also in type II ganglion cells, their peripheral and central processes and in outer hair cell terminals. The stained cell bodies were smaller than the unstained type I ganglion cells and they were much fewer in number. The processes of the stained cells could be followed from the soma. The central processes were dispersed throughout the VIIIth nerve trunk. Stained peripheral processes were evident in the osseous spiral lamina, floor of the tunnel of Corti and first space of Nuel and in the outer spiral plexus along the sides of the outer phalangeal (Deiters') cells. AChE-stained afferent terminals were easy to identify after transection of the crossed olivocochlear bundle (COCB) and subsequent degeneration of large efferent terminals. These results are of interest in that assessments of efferent nerve histochemistry after COCB transection need to recognize the potential contribution of AChE reaction product in afferent terminals.(ABSTRACT TRUNCATED AT 250 WORDS)

Acetylcholinesterase

Imaging the cochlea by magnetic resonance microscopy.

The isolated, fixed cochlea of the mustached bat was studied with three dimensional magnetic resonance (MR) microscopy. The cochlea of this animal is about 4 mm in diameter and its entire volume was imaged. With the field of view and matrix size used, the volume elements (voxels) making up the volume data set were isotropic 25 x 25 x 25 micron cubes. Three dimensional (3D) MR microscopy based on isotropic voxels has many advantages over commonly used light microscopy: 1) it is non destructive; 2) it is much less time consuming; 3) no dehydration is required and shrinkage is minimized; 4) the data set can be used to create sections in any desired plane; 5) the proper alignment of sections is inherent in the 3D acquisition so that no reference points are required; 6) the entire data set can be viewed from any point of view in a volume rendered image; 7) the data is digital and features can be enhanced by computer image processing; and 8) the isotropic dimensions of the voxels make the data well-suited for structural reconstructions and measurements. Good images of the osseous spiral lamina, spiral ligament, scala tympani, scala vestibuli, and nerve bundles were obtained. The vestibular (Reissner's) membrane was easily identified in the mustached bat and it appears to bulge into the scala vestibuli. The visibility of this structure suggests that MR microscopy would be well-suited for studies of endolymphatic hydrops.

Animals

Cell types in the mustached bat auditory cortex.

Cells in the auditory cortex of the mustached bat were studied with Golgi stains. No cell types appeared to be unique to the mustached bat auditory cortex or to specialized functional areas, but the laminar proportions and distributions of cell types were somewhat different from that reported for primary sensory cortex of other species. Two major cell types were distinguished, those with dendritic spines and those without spines. Non-spiny neurons were concentrated deep in layer III/IV and in layer V, and had three types of dendritic patterns, multipolar, bitufted and bipolar. Many of the non-spiny neurons were large; some nearly equaled the largest pyramidal neurons in size. Five types of spiny neurons were identified, pyramidal cells, extraverted pyramidal cells, 'spiny stellate-like' neurons, and multiform cells. In the narrow, densely packed, 'accentuated' layer II, slightly more than half of the spiny neurons were extraverted pyramidal cells, which are characterized by multiple, widely diverging apical dendrites. The high concentration of layer II extraverted pyramidal neurons is consistent with descriptions of the 'accentuated' layer II previously reported in other bat species and 'basal' insectivores. The remaining spiny neurons in layer II, and the preponderance of spiny neurons in layers III-VI, were typical pyramidal neurons that had single apical dendrites and tufts of basal dendrites. The thalamic recipient zone (deep layer III/IV) contained few candidates for spiny stellate cells, so a major constituent of the thalamic recipient zone in primary sensory cortex of many species is only a minor cellular component in the mustached bat auditory cortex.

Animals

Doppler-shift compensation by the mustached bat: quantitative data.

Quantitative data for Doppler-shift compensation by Pteronotus parnellii parnellii were obtained with a device which propelled the bats at constant velocities over a distance of 12 m. The bats compensated for Doppler shifts at all velocities tested (0.1-5.0 ms-1). The main findings were (1) that compensation was usually accomplished by a progressive lowering of the approximately 61 kHz second harmonic constant-frequency component of emitted sounds in small frequency steps (93 +/- 72 Hz); (2) that the time needed to reach a steady compensation level averaged 514 +/- 230 ms and the number of pulses required to reach full compensation averaged 10.78 +/- 5.16; (3) that the animals compensated to hold the echo (reference) frequency at a value that was slightly higher than the resting frequency and slightly lower than the cochlear resonance frequency; (4) that reference frequency varied as a function of velocity, the higher the velocity of the animal, the higher was the reference frequency (slope 55 Hz m-1s-2); and (5) that the mean reference frequency was always an undercompensation. The average amount of undercompensation was 15.8%. There was a significant difference (P < or = 0.005) in Doppler-shift compensation data collected at velocities that differed by 0.1 ms-1. A velocity difference of 0.1 ms-1 corresponds to a Doppler-shift difference of about 35 Hz in the approximately 61 kHz signals reaching the ear.

Acoustics

Labile cochlear tuning in the mustached bat. I. Concomitant shifts in biosonar emission frequency.

The cochlea of the mustached bat (Pteronotus parnellii) has sharp tuning characteristics and pronounced resonance within a narrow band near the second harmonic, constant frequency (CF2) component of the animal's biosonar signals. That fine frequency discrimination occurs within this narrow band is evident from Doppler-shift compensation, whereby bats in flight lower the frequency of emitted CF2s to maintain returning echoes within this band. This study examined various factors capable of producing shifts in both the cochlear resonance frequency (CRF) and CF2s emitted by stationary bats and bats actively Doppler-shift compensating on a pendulum. Each of three experimental factors shifted the CRF in a reversible manner. Changes in body temperature produced an average CRF shift of 39 +/- 18 Hz/degrees C. The CRF increased with flight by 150 +/- 100 Hz and returned to baseline values within 10 min after flight. Contralateral sound exposure produced smaller (100 +/- 20 Hz), rapid shifts in the CRF, suggesting that a mechanism different from the temperature- and flight-related shifts was involved. Changes in the CRF induced by temperature and flight were accompanied by shifts in the emitted CF2 of stationary and moving bats. Coupled with a companion study of associated shifts in neural tuning, the concomitant changes in CRF and CF2 provide evidence of cochlear tuning lability in the mustached bat.

Acoustic Stimulation

Labile cochlear tuning in the mustached bat. II. Concomitant shifts in neural tuning.

Acoustic stimuli near 60 kHz elicit pronounced resonance in the cochlea of the mustached bat (Pteronotus parnellii parnellii). The cochlear resonance frequency (CRF) is near the second harmonic, constant frequency (CF2) component of the bat's biosonar signals. Within narrow bands where CF2 and third harmonic (CF3) echoes are maintained, the cochlea has sharp tuning characteristics that are conserved throughout the central auditory system. The purpose of this study was to examine the effects of temperature-related shifts in the CRF on the tuning properties of neurons in the cochlear nucleus and inferior colliculus. Eighty-two single and multi-unit recordings were characterized in 6 awake bats with chronically implanted cochlear microphonic electrodes. As the CRF changed with body temperature, the tuning curves of neurons sharply tuned to frequencies near the CF2 and CF3 shifted with the CRF in every case, yielding a change in the unit's best frequency. The results show that cochlear tuning is labile in the mustached bat, and that this lability produces tonotopic shifts in the frequency response of central auditory neurons. Furthermore, results provide evidence of shifts in the frequency-to-place code within the sharply tuned CF2 and CF3 regions of the cochlea. In conjunction with the finding that biosonar emission frequency and the CRF shift concomitantly with temperature and flight, it is concluded that the adjustment of biosonar signals accommodates the shifts in cochlear and neural tuning that occur with active echolocation.

Acoustic Stimulation

Efferent terminals in the cochlea of the mustached bat: quantitative data.

Efferent terminals in the cochlea of the mustached bat were stained for acetylcholinesterase (AChE) and quantitative data were obtained for the number and size of the endings on the outer hair cells (OHCs) in each row, from base to apex. From TEM micrographs and AChE-stained, surface preparations it was determined that every OHC had a single, large terminal. The mean size of the terminals was significantly different in each row, with the largest occurring in the first row (7.1 microns 2); the mean size in the second and third rows was 5.7 and 5.0 microns 2 respectively. In specific frequency processing regions, the largest mean size (8.4 microns 2) for first row OHCs was consistently found in the distal densely innervated (DDI) area. This region has afferent neurons that are sharply tuned to the second harmonic, constant frequency component of the bat's biosonar signals. Sudden changes in the size of the terminals were observed exactly at the boundaries of the DDI with adjacent sparsely innervated regions. Similar, but less striking, size changes also occurred in and adjacent to the proximal densely innervated (PDI) region, a harmonically related, sharply tuned region, which processes the bat's 91.5 kHz, third harmonic, constant frequency signals. The region of the cochlea with the smallest first row terminals (mean 5.3 microns 2) was the large, sparsely innervated region of the basal turn, a region that does not appear to process biosonar signals. Although the significance of differences in efferent terminal size is not known, the data suggest a possible correlation between OHC stimulation and sharp tuning. The potentially greater influence of the efferent fibers on the first row of OHCs, compared to other rows, is consistent with observations made on other mammals; in the latter, however, the greater influence has been suggested more by number than size. Unlike other mammals, the OHC efferents in the mustached bat have no clear base-to-apex gradient in the number or size of the efferent terminals. It is suggested that this might reflect the high frequency nature of the ear (6-120 kHz) and absence of low frequency hearing.

Acetylcholinesterase

Contractile proteins in the hyaline cells of the chicken cochlea.

Hyaline cells are a single layer of epithelial cells found at the inferior edge of the sensory epithelium in the chick cochlea. They rest directly above a specialized region of the basilar membrane at a point where it connects to the fibrocartilaginous skeleton of the cochlear duct. The basal cytoplasm of the hyaline cells contains a bundle of linearly aligned actin filaments that resemble stress fibers in their organization. The actin filaments are anchored in the basal plasma membranes of the cells, which are, in turn, associated with the underlying basal lamina and the extracellular matrix of the basilar membrane. We have used a combination of transmission electron microscopy, differential-interference-contrast and epifluorescence light microscopy, and confocal laser scanning microscopy to study the composition and organization of these actin bundles within the hyaline cells. The bundles are arranged into triangular wedges that are oriented radially across the basilar membrane. Each cell contains one or two actin wedges. Adjacent cells can have them aligned in opposite directions so that in a whole-mount surface preparation they appear as interdigitations. Immunofluorescent staining of the hyaline cells has shown that smooth muscle myosin and alpha-actinin are co-localized to the actin bundles. Smooth muscle myosin is also found throughout the cytoplasm of the cells. The fact that hyaline cells in the chick cochlea are contacted by efferent nerve fibers suggests that these cells may regulate tension on the basilar membrane via the specialized bundle of actin filaments.

Animals

Ultrasonic vocalizations of flying bats monitored by radiotelemetry.

Ultrasonic vocalizations of flying bats were effectively monitored with radiotelemetry. We describe a device light enough to be carried by an 11 g bat for periods of up to 1 h. It transmitted signals adequate for fine frequency analysis within a range of approximately 3 m. Telemetry permitted the recording of constant-frequency pulses free from flight-induced Doppler shifts and without time delays. The difference in frequency between telemetered signals and the same signals detected by a remote microphone was used to calculate velocity and Doppler shifts. Pulse emission behavior of Pteronotus parnellii in flight was compared with simulated flight on a pendulum. The data showed significant differences in echo bandwidths, constant-frequency pulse durations and interpulse intervals. In flight, pulses and interpulse intervals tended to be shorter and bats maintained echo frequencies within a significantly narrower band. Phases of echolocation that characterized the approach to a target were clearly evident in flight, but not during pendulum swings. Differences in pulse durations and interpulse intervals may be correlated with the integration of wingbeat, respiration and vocalization. The absence of wing motion in simulated flight changes this integration.

Animals

Course and distribution of efferent fibers in the cochlea of the mouse.

The course, distribution and termination of single efferent fibers to the cochlea has been described in only a few animals and relatively few fibers have been studied with knowledge of their ipsilateral or contralateral origin. In order to examine the efferent fibers in the mouse, the anterograde tracer Phaseolus vulgaris leucoagglutinin (PHA-L) was iontophoretically injected into one side of the brain stem near the location of known efferent nuclei. Examination of surface preparations of the cochlea revealed detailed information for both the lateral olivocochlear (LOC) and medial olivocochlear (MOC) systems. Many, but not all, fibers entered the cochlea within the intraganglionic spiral bundle (IGSB). The LOC fibers were restricted to the ipsilateral cochlea and rarely branched within the IGSB and osseous spiral lamina (OSL). In the organ of Corti, they traveled either basally or apically in the region of the inner hair cells (IHCs), spanning lengths up to 130 microns (basally) and 890 microns (apically). Terminal swellings of these fibers were ca 3.0 microns in diameter. Numerous en passant swellings were present where the fibers formed a plexus in the area of the IHCs. The MOC fibers followed a similar course in the IGSB and OSL, and within the OSL the fibers had few branches. Within the organ of Corti they traveled apically (up to 70 microns) in the nerve bundles located in the IHC area before they crossed the tunnel of Corti. In the region of the OHCs, 9% of the traceable fibers branched to innervate two to three OHCs while 91% appeared to innervate only one OHC. There was no discernible difference in the distribution of contralateral and ipsilateral MOC projections in terms of cochlear region or outer hair cell rows.

Animals

Cochlear and CNS tonotopy: normal physiological shifts in the mustached bat.

The ear of the mustached bat (Pteronotus parnellii) shows marked cochlear resonance near 60 kHz and many sharply tuned neurons throughout the brain have best frequencies (BF) near the cochlear resonance frequency (CRF). Controlled changes in the normal physiological range of body temperature (approx 37-42 degrees C) were used to change the CRF and to study the tuning properties of neurons in the cochlear nucleus (CN) and inferior colliculus (IC). In all cases there were concomitant shifts in the CRF and the BFs. Results were the same for single and multi-units, and for CN and IC units. Although the BF reliably changed with shifts in the CRF, the majority of the units showed no change in minimum threshold or the sharpness (Q10 dB) of tuning. The temperature-induced effects on cochlear tuning were similar to those previously described in nonmammalian vertebrates. The physiological data reveal that, within a narrow frequency band, cochlear and CNS tonotopy are labile in the mustached bat. The lability of tuning is further substantiated by adaptations of biosonar emission behavior with shifts in CRF (Henson et al., 1990).

Acoustic Stimulation

Specializations for sharp tuning in the mustached bat: the tectorial membrane and spiral limbus.

The sense of hearing in the mustached bat, Pteronotus parnellii, is specialized for fine frequency analysis in three narrow bands that correspond to approx 30, 60 and 90 kHz constant frequency harmonics in the biosonar signals used for Doppler-shift compensation and acoustic imaging of the environment. Previous studies have identified anatomical specializations in and around the area of the cochlea that processes the dominant second harmonic component, but similar features have not been found in areas related to sharp tuning and high sensitivity for the first or third harmonics. In this report we call attention to the large size of the tectorial membrane and spiral limbus in all three areas that appear to process the harmonically related constant frequency components. These structures are especially pronounced in the regions of the cochlea that respond to the approx 61 kHz, second harmonic and 91.5 kHz, third harmonic bands; they correspond specifically to areas where the density of afferent nerve fibers is high and where very sharply tuned neurons occur. These data for cochleae with multiple specializations lend strong support to the idea that the mass of the tectorial membrane can be an important factor in establishing the response properties of the cochlea.

Animals

Cochlear resonance in the mustached bat: behavioral adaptations.

Mustached bats, Pteronotus p. parnellii, use complex, multiharmonic biosonar signals with prominent approx. 60 kHz (CF) components. The sense of hearing is especially acute to sounds near 60 kHz and the cochlea shows a number of specializations in the 60 kHz region. Foremost is a remarkable degree of cochlear resonance. In this study it is shown that: 1) any sounds near the resonance frequency elicit a pronounced resonance that continues after the stimulus terminates; 2) Doppler-shifted echoes of the bat's own cries may cause resonance; 3) continuous resonance can be produced by stimulating the ear with broadband noise but such resonance does not interfere with the bat's ability to Doppler-shift compensate during simulated flight; 4) significant changes in the resonance frequency of the cochlea occur during and after flight; 5) the changes in resonance can be dependent or independent of body temperature changes; and 6) mustached bats continuously adjust the CF component of their pulses to keep the second harmonic echoes in a constant frequency band near the resonance frequency. Thus, mustached bats not only compensate for Doppler-shifts imposed by their movements relative to that of a target, but they cochlear resonance compensate to deal with small changes in the micromechanical properties of the cochlea.

Animals