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Anatomical and physiological investigation of auditory input to the superior colliculus of the echolocating megachiropteran bat Rousettus aegyptiacus.

The objective of this study was to investigate whether a representation of auditory space in the superior colliculus (SC) of the echolocating megachiropteran bat (Rousettus aegyptiacus) exists. Additionally the subcortical auditory connectivity of the SC was investigated. A total of 207 units were recorded in five awake animals while presenting acoustic stimuli (white noise, clicks, and pure tones) at different positions in space. Six units responded to acoustic stimulation. Three of these located within the superficial layers and one located in the intermediate layers were classified as omnidirectional units. Two units were located within the deep layers. One was classified as a hemifield unit, and the other as a frontal unit. All units responded phasically to acoustic stimulation with a latency of 4-150 ms. None of them could be activated by visual stimuli. We further examined the interaction of paired auditory and visual stimulation in 116 visually responsive units. Responses to visual stimulation were markedly altered by acoustic stimulation in 5 units. The influence of the acoustic stimuli was temporally and spatially restricted, and resulted either in a reduction or an elevation of unit responsiveness. Horseradish peroxidase was injected into the SC of eight animals to investigate the auditory subcortical connectivity of the SC. Retrograde labeling in auditory structures was rare compared with labeling found in nonauditory structures (e.g., retina, substantia nigra, parabigeminal nucleus). In auditory structures retrograde labeling was found mainly in the external nucleus of the inferior colliculus and in the nucleus of the brachium of the inferior colliculus. To a lesser extent it was found in the nucleus sagulum and in the area medial to the lemniscal nuclei. In one case the dorsal nucleus of the lateral lemniscus and the anterolateral periolivary nucleus were labeled. Our results reveal only a sparse auditory input into the SC of the flying fox, R. aegyptiacus. On the basis of single-unit recordings, we did not find an elaborate representation of auditory space as it is described for several other species. The existence of auditory and bimodal neurones, in combination with their response properties, nonetheless indicate that there might be a representation of auditory space in the SC of R. aegyptiacus.

Acoustic Stimulation↗

The pineal gland of nocturnal mammals. II. The ultrastructure of the pineal gland in the pipistrelle bat (Pipistrellus pipistrellus L.): presence of two populations of pinealocytes.

In the pineal gland of the pipistrelle bat two different populations of pinealocytes and glial cells were observed electron microscopically. The pinealocytes of populations I and II differ in their content of metabolically active cell organelles. In the pinealocytes of population I, granular vesicles originating from the Golgi apparatus were found in the perikaryon and especially in the endings of the pinealocyte processes. Granular vesicles appeared to be more numerous in hibernating nulliparous females. The pinealocytes of population II are characterized by the presence of small cytoplasmic vacuoles, probably originating from cisternae of the granular endoplasmic reticulum and containing flocculent material of moderate electron density. The classification of the pinealocytes belonging to population II is discussed.

Animals↗

A histochemical study on the innervation of the cerebral blood vessels in bats.

The adrenergic and cholinergic nerves innervating the cerebral blood vessels of four species of Japanese chiropterids (Rhinolophus ferrumequinum, Murina leucogaster, Vespertilio superans and Miniopterus schreibersi) have been investigated using specific histochemical techniques. In all these species of bats arteries of the internal carotid system are poorly developed, whereas those of the vertebro-basilar system are well developed. The adrenergic and cholinergic nerves innervating these cerebral arteries, however, all originate from the stem nerve bundles entering the cranial cavity along the internal carotid artery. Both nerve plexuses are among the densest of any vertebrate species so far investigated. Adrenergic nerve plexuses are usually composed of complicated meshworks of fine fibres, while cholinergic ones are composed of rather longitudinally arranging meshworks of both thick and thin fibres, exhibiting a very high acetylcholinesterase activity. Small parenchymal arteries and arterioles are also dually innervated by adrenergic and cholinergic nerve fibres of peripheral origin. Intracerebral capillaries, on the other hand, are in several places directly connected with both adrenergic and cholinergic fibres of parenchymal origin. Capillaries in the cerebral and cerebellar cortices, diencephalon and cochlear nucleus in v. superans exhibit a heavy non-nervous acetylcholinesterase activity in their walls, but in R. ferrumequinum and M. schreibersi, the response is weak or negative, except for that in the cochlear nucleus.

Acetylcholinesterase↗

Changes in the fine structure of the testicular Leydig cells of the seasonally-breeding bat, Myotis adversus.

Leydig cells of the bat, Myotis adversus, have been examined by electron microscopy throughout fourteen months. During the breeding season the Leydig cells become hypertrophied and are characterised by prominent areas of agranular endoplasmic reticulum and numerous small, membrane-bound granules. Microperoxisomes are also observed. During the period of testicular regression. Leydig cell size and the number of membrane-bound granules are greatly reduced. Lipid droplets and dense bodies are more numerous.

Animals↗

Changes in milk composition during lactation in three species of insectivorous bats.

Changes in milk composition are described for three species of free-ranging insectivorous bats (Myotis lucifugus, M. velifer, and Tadarida brasiliensis) from early to mid (peak) lactation. Dry matter and energy concentrations in milk increased from early to mid-lactation. In M. lucifugus and T. brasiliensis, but not M. velifer, these increases were due largely to a rise in fat concentration, since protein and carbohydrate remained relatively constant. Energy content of milk (kJ.g-1) for each species from early through mid-lactation was related to dry matter (DM) as follows: M. lucifugus (y = 0.31 DM-0.32, r2 = 0.68), M. velifer (y = 0.48 DM-5.08, r2 = 0.99), and T. brasiliensis (y = 0.37 DM-1.51, r2 = 0.61). Comparison of the effect of sampling method on milk composition of T. brasiliensis indicated that fat, dry matter, and energy concentrations increased significantly from pre-dawn to pre-noon samples. Relatively high fat and low water levels in T. brasiliensis milk may reflect the limited access that lactating females have to free water, as well as need to minimize mass of stored milk during long foraging trips. Conversely, lower fat concentrations and higher water levels in milk in M. lucifugus and M. velifer may relate to the propensity for colonies of these two species to roost and forage near bodies of water. In addition, differences in milk fat concentrations observed among the three species may correlate to daily suckling schedules.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗

The functional significance of ventilation frequency, and its relationship to oxygen demand in the resting brown long-eared bat, Plecotus auritus.

Mean oxygen consumption and simultaneous ventilation frequency of nine non-reproductive brown long-eared bats (body mass 8.53-13.33 g) were measured on 159 occasions. Ambient (chamber) temperature at which the measurements were made ranged from 10.8 to 41.1 degrees C. Apneic ventilation occurred in 22 of the 59 measurements made when mean oxygen consumption was less than 0.5 ml.min-1. No records of apneic ventilation were obtained when it was over 0.5 ml.min-1. The relationship between ventilation frequency and mean oxygen consumption depended on whether ventilation was apneic or non-apneic. When ventilation was non-apneic the relationship was positive and log-linear. When ventilation was apneic the relationship was log-log. Within the thermoneutral zone ventilation frequency was not significantly different from that predicted from allometric equations for a terrestrial mammal of equivalent body mass, but was significantly greater than that predicted for a bird. A reduction in the amount of oxygen consumed per breath occurred at ambient temperatures above the upper critical temperature (39 degrees C).

Animals↗

Response properties of FM-FM combination-sensitive neurons in the auditory cortex of the mustached bat.

For echolocation, the mustached bat, Pteronotus parnellii rubiginosus, emits orientation sounds (pulses) and listens to echoes. Each pulse is made up of 8 components, of which 4 are constant frequencies (Cf 1.4) and 4 are frequency-modulated (FM 1-4). Target-range information, conveyed by the time delay of the echo FM from the pulse FM, is processed in this species by specialized neurons in a part of the auditory cortex known as the FM-FM area. These cortical neurons are responsive to pulse-echo pairs at specific echo delays. The essential components in the sound pair include the pulse FM1 followed by an echo FMn (n = 2, 3 or 4). Downward sweeping FM1-FMn sounds that are similar to those the animal naturally hears during echolocation are the most effective in evoking facilitative responses. Most FM-FM neurons, however, still exhibit facilitative responses to stimulus pairs consisting of upward sweeping FM sounds and/or pure tones at frequencies found in FM sweeps. The magnitude of facilitation is altered by changes in echo rather than pulse amplitude. Neurons characterized by shorter best delays (or echoes from closer targets) do not require larger best echo amplitudes for facilitation.

Animals↗

Control of echolocation pulses by neurons of the nucleus ambiguus in the rufous horseshoe bat, Rhinolophus rouxi. II. Afferent and efferent connections of the motor nucleus of the laryngeal nerves.

Horseradish peroxidase was applied by inotophoretic injections to physiologically identified regions of the laryngeal motor nucleus, the nucleus ambiguus in the CF/FM bat Rhinolophus rouxi. The connections of the nucleus ambiguus were analysed with regards to their possible functional significance in the vocal control system, in the respiration control system, and in mediating information from the central auditory system. The nucleus ambiguus is reciprocally interconnected with nuclei involved in the generation of the vocal motor pattern, i.e., the homonomous contralateral nucleus and the area of the lateral reticular formation. Similarly, reciprocal connections are found with the nuclei controlling the rhythm of respiration, i.e., medial parts of the medulla oblongata and the parabrachial nuclei. Afferents to the nucleus ambiguus derive from nuclei of the 'descending vocalization system' (periaqueductal gray and cuneiform nuclei) and from motor control centers (red nucleus and frontal cortex). Afferents to the nucleus ambiguus, possibly mediating auditory influence to the motor control of vocalization, come from the superior colliculus and from the pontine nuclei. The efferents from the pontine nuclei are restricted to rostral parts of the nucleus ambiguus, which hosts the motoneurons of the cricothyroid muscle controlling the call frequency.

Afferent Pathways↗

The nuclei of the lateral lemniscus in the rufous horseshoe bat, Rhinolophus rouxi. A neurophysiological approach.

In the rufous horseshoe bat, Rhinolophus rouxi, responses to pure tones and sinusoidally frequency modulated (SFM) signals were recorded from 289 single units and 241 multiunit clusters located in the nuclei of the lateral lemniscus (NLL). The distribution of best frequencies (BFs) of units in all three nuclei of the lateral lemniscus showed an overrepresentation in the range corresponding to the constant-frequency (CF) part of the echolocation signal ('filter frequency' range): in the ventral nucleus of the lateral lemniscus (VNLL) 'filter neurons' represented 43% of all units encountered, in the intermediate nucleus (INLL) 33%, and in dorsal nucleus (DNLL) 29% (Fig. 2a). Neurons with best frequencies in the filter frequency range had highest Q10dB-values (maxima up to 400, Fig. 2c) and only in low-frequency units were values comparable to those found in other mammals. On the average, filter neurons in ventral nucleus had higher Q10dB-values (about 220) than did those in intermediate and dorsal nucleus (both about 160, Fig 2d). Response patterns and tuning properties showed higher complexity in the dorsal and intermediate nucleus than in the ventral nucleus of the lateral lemniscus (Figs. 4 and 6). Multiple best frequencies were found in 12 neurons, nine of them with harmonically related excitation maxima (Fig. 5c, d). Best frequencies of six of these harmonically tuned units could not be correlated with any harmonic components of the echolocation signal. Half of all multiple tuned neurons were located in the caudal dorsal nucleus the other half in the caudal intermediate nucleus. Synchronization of responses to sinusoidally frequency modulated (SFM) signals occurred in VNLL-units in the average up to modulation frequencies of 515 Hz (maximum about 800 Hz) whereas in the intermediate and dorsal nucleus of the lateral lemniscus responses were synchronized in the average only up to modulation frequencies of about 300 Hz (maximum about 600 Hz) (Figs. 7 and 8). A tonotopic arrangement of units was found in the intermediate nucleus of the lateral lemniscus with units having high best frequencies located medially and those with low best frequencies laterally. In the dorsal nucleus the tonotopic distribution was found to be fairly similar to that in the intermediate nucleus but much less pronounced. In more rostral parts of the dorsal nucleus additionally higher best frequencies predominated whereas in caudal areas of that nucleus and also of the intermediate nucleus low BFs were found more regularly.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Frequency sensitivity and directional hearing in the gleaning bat, Plecotus auritus (Linnaeus 1758).

1. The neural audiogram of the common long-eared bat, Plecotus auritus was recorded from the inferior colliculus (IC). The most sensitive best frequency (BF) thresholds for single neurones are below 0 dB SPL between 7-20 kHz, reaching a best value of -20 dB SPL between 12-20 kHz. The lower and upper limits of hearing occur at 3 kHz and 63 kHz, respectively, based on BF thresholds at 80 dB SPL. BF threshold sensitivities are about 10 dB SPL between 25-50 kHz, corresponding to the energy band of the sonar pulse (26-78 kHz). The tonotopic organization of the central nucleus of the IC (ICC) reveals that neurones with BFs below 20 kHz are disproportionately represented, occupying about 30% of ICC volume, occurring in the more rostral and lateral regions of the nucleus. 2. The acoustical gain of the external ear reaches a peak of about 20 dB between 8-20 kHz. The gain of the pinna increases rapidly above 4 kHz, to a peak of about 15 dB at 7-12 kHz. The pinna gain curve is similar to that of a simple, finite length acoustic horn; expected horn gain is calculated from the average dimensions of the pinna. 3. The directional properties of the external ear are based on sound diffraction by the pinna mouth, which, to a first approximation, is equivalent to an elliptical opening due to the elongated shape of the pinna. The spatial receptive field properties for IC neurones are related to the directional properties of the pinna. The position of the acoustic axis of the pinna and the best position (BP) of spatial receptive fields are both about 25 degrees from the midline between 8-30 kHz but approach the midline to 8 degrees at 45 kHz. In elevation, the acoustic axis and the BP of receptive fields move upwards by 20 degrees between 9-25 kHz, remaining stationary for frequencies up to 60 kHz. 4. The extremely high auditory sensitivity shown by the audiogram and the directionality of hearing are discussed in terms of the adaptation of the auditory system to low frequencies and the role of a large pinna in P. auritus. The functional significance of low frequency hearing in P. auritus is discussed in relation to hunting for prey by listening and is compared to other gleaning species.

Acoustic Stimulation↗

Autoradiographic quantification of muscarinic cholinergic synaptic markers in bat, shrew, and rat brain.

We employed radioligand binding autoradiography to determine the distributions of pre- and post-synaptic cholinergic radioligand binding sites in the brains of two species of bat, one species of shrew, and the rat. High affinity choline uptake sites were measured with [3H]hemicholinium, and presynaptic cholinergic vesicles were identified with [3H]vesamicol. Muscarinic cholinergic receptors were determined with [3H]scopolamine. The distribution patterns of the three cholinergic markers were similar in all species examined, and identified known major cholinergic pathways on the basis of enrichments in both pre- and postsynaptic markers. In addition, there was excellent agreement, both within and across species, in the regional distributions of the two presynaptic cholinergic markers. Our results indicate that pharmacological identifiers of cholinergic pathways and synapses, including the cholinergic vesicle transport site, and the organizations of central nervous system cholinergic pathways are phylogenetically conserved among eutherian mammals.

Animals↗

The pineal gland of nocturnal mammals. I. The pinealocytes of the bat (Nyctalus noctula, Schreber).

The ultrastructure of the pinealocytes of noctule bats, mammals which live most of the time in darkness or very low light intensities, was examined and compared with the pinealocytes of other mammals. Two different populations of pinealocytes (I and II) were observed. They differ in general aspect, in location and especially in their content of cell organelles involved in synthetic processes. Mitochondria, ribosomes, lysosomes and lipid inclusions were present in the perikaryon of pinealocytes of both populations. In the pinealocytes of population I some granular vesicles, of presumed Golgi origin, and some other structures were observed. Pinealocytes of population II are characterized by many glycogen granules, more or less associated with a large vacuolar system. Moreover, some small vacuoles originating from cisterns of the granular endoplasmic reticulum and containing flocculent material of a moderate electron density are described. The possibility is discussed that these small vacuoles are involved in one of the secretory processes of the pineal gland while the granular vesicles of the pinealocyte of the population I are the products of another.

Animals↗

Acoustical and neural aspects of hearing in the Australian gleaning bats, Macroderma gigas and Nyctophilus gouldi.

1. The maximum acoustic gain of the external ear in Macroderma gigas was found to be 25-30 dB between 5-8 kHz and in Nyctophilus gouldi it reached 15-23 dB between 7-22 kHz. Pinna gain reached a peak of 16 dB near 4.5-6 kHz in M. gigas and 12-17 dB between 7-12 kHz in N. gouldi, with average gain of 6-10 dB up to 100 kHz. Pinna gain curves resemble that of a finite conical horn, including resonance. 2. The directional properties of the external ear in both species result from sound diffraction at the pinna face, as it approximates a circular aperture. The frequency dependent movement of the acoustic axis in azimuth and elevation is attributed to the asymmetrical structure of the pinnae. 3. Evoked potentials and neuronal responses were studied in the inferior colliculus. In M. gigas, the neural audiogram has sensitivity peaks at 10-20 kHz and 35-43 kHz, with extremely low thresholds (-18 dB SPL) in the low frequency region. In N. gouldi, the neural audiogram has sensitivity peaks at 8-14 kHz (lowest threshold 5 dB SPL) and 22-45 kHz. Removal of the contralateral pinna causes a frequency dependent loss in neural threshold sensitivity of up to 10-15 dB in both species. 4. The high frequency peak in the audiogram coincides with the sonar energy band in both species, whereas the low frequency region is used for social communication. Highly sensitive low frequency hearing is discussed in relation to hunting in bats by passive listening.

Acoustic Stimulation↗

Fine structure of the XY body in the XY1Y2 trivalent of the bat Artibeus lituratus.

Electron microscopy of spread spermatocytes and thin sections has been used to study the sex trivalent (XY1Y2) of the bat Artibeus lituratus. Pachytene spermatocytes in thin sections show an XY body with typical chromatin condensation that is connected to autosomal chromatin through a synaptonemal complex (SC). Microspread spermatocytes show three axes and two SC segments (a short SC and a long one) in the sex trivalent. The short paired region corresponds to synapsis between the 'original' X and Y pieces, while the long paired region corresponds to synapsis between the Y2 element and the homologous, autosomal piece of the compound X-chromosome. The length ratios of the three axes correspond to those of the three mitotic chromosomes, X, Y1 and Y2. The high packing of chromatin corresponds exclusively to the 'original' pieces of the X and Y elements, while the autosomal regions of the X and the Y2 axes are surrounded by autosomal-like chromatin. Thus, in this trivalent the formation of an XY body in the 'original' sex chromosomes is not inhibited by the presence of the autosomal pieces, and typical partial synapsis between the original X and Y elements is conserved. C-banding heterochromatin seems not to be the barrier preventing the spreading of heterochromatinization towards the autosomal piece in this trivalent.

Animals↗

Immunocytochemical localization of vasoactive intestinal polypeptide (VIP) in the brain of the little brown bat (Myotis lucifugus).

Vasoactive intestinal polypeptide (VIP)-like immunoreactivity has been examined in the brain of the little brown bat, Myotis lucifugus, using light microscopic immunocytochemistry and the indirect antibody enzyme method of Sternberger. Animals were sacrificed at three different and discrete levels of physiological activity: euthermic, hypothermic and hibernating. The density and distribution of immunoreactive neurons and fibres was compared in the three animal groups with the aid of a computerized image analysis system. Our results were compared with those of previous studies in laboratory species such as the rat and cat. Our study has demonstrated marked changes in the density of VIP-immunoreactive fibres and plexuses in the anterior hypothalamic area which correspond to the physiological state of the animal. In addition we have demonstrated the presence of VIP immunoreactive perikarya in a number of previously unreported locations. These include the paraventricular and periventricular hypothalamic nuclei, the linear raphe nucleus, nucleus interfascicularis, and in neurons embedded in the fibres of the dorsal tegmental decussation.

Animals↗

Comparative study of the karyotypes of two Egyptian species of bats, Taphozous perforatus and Taphozous nudiventris (Chiroptera: Mammalia).

A detailed karyotypic analysis of two Egyptian species of bats, Taphozous perforatus and Taphozous nudiventris, was made on the basis of conventional data and G-band patterns. No detectable karyotypic difference was found between the two species (2n = 42, F. N. 64). By comparison of G-band patterns, some differences between the two species were seen in the corresponding autosomal pairs. These results are reported for the first time in Egypt.

Animals↗

Electrical response of bat retina to spectral stimulation: comparison of four microhiropteran species.

Electrical responses of the retinas of 4 species of microchiropteran bats stimulated by spectrally restricted light flashes were found to diverge systematically from the rhodopsin absorption spectrum. The divergence was progressively greater across the 4 species. The results appeared explainable by assuming a second photoreceptor class and photopigment which was present in progressively greater numbers in the retinas of Eptesicus fuscus, Desmodus rotundus, Artibeus jamaicensis and Carollia perspicillata.

Animals↗