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Auditory response properties and directional sensitivity of cerebellar neurons of the echolocating bat, Eptesicus fuscus.

Auditory response properties and directional sensitivity of cerebellar neurons of Eptesicus fuscus were studied under free-field stimulation conditions. The best frequency (BF) and minimum threshold (MT) of a recorded neuron were first determined with a sound delivered in front of the bat. Discharge pattern and MT were studied with both BF stimuli and one-octave downward and upward sweep FM (frequency-modulated) stimuli. The directional sensitivity of cerebellar neurons was then studied by determining the variation of MT and response latency with BF and FM stimuli broadcast from each of 15 loudspeakers attached to a semicircular wooden track in front of the bat. All 85 cerebellar neurons recorded discharged phasically to acoustic stimuli. Only 20 were spontaneously active. Cerebellar neurons were generally more sensitive to FM stimuli than to pure tone pulses. Thus, they discharged more vigorously and had a lower MT to the former than the latter stimulus. Directional sensitivity of 47 neurons (BF = 23.4-81.1 kHz) was studied. All neurons varied their MTs with sound direction. Most neurons (n = 37, 79%) showed a lowest MT to a frontal sound. Directional sensitivity of cerebellar neurons appears to be sharper when determined with BF tone pulses than with FM stimuli. Thus the directional slope and the difference in MT between the best and worst angles of these neurons were larger when determined with the BF stimulus. Directional sensitivity of cerebellar neurons is not dependent upon stimulus frequency, unlike that of the inferior and cortical neurons of the same bat. Cerebellar neurons also varied their response latency with sound direction. Such a variation may provide the bat with another neural code for sound localization.

Animals↗

Pulmonary design in a microchiropteran bat (Pipistrellus subflavus) during hibernation.

The Eastern pipistrelle (Pipistrellus subflavus) is typical of exceptionally small bats capable of a 30-fold range in aerobic metabolism as they arouse from hypothermia and sustain foraging flight. This report describes their basic lung structure and the extent to which this organ is protected from protein depletion during hibernation. Bats were collected at the beginning (Fall), middle (Winter), and end (Spring) of hibernation from a permanent overwintering cave, and analyzed within several days of capture. Regardless of whether bats were examined in the Fall (average body weight = 6.22 g) or in the Spring (4.58 g) no significant differences existed for total lung volume (237 microliter), alveolar surface area (338 cm2), harmonic mean septal thickness, tau ht (0.221 micron), or membrane diffusing capacity (4.13 microliter O2/sec/mbar). These parameters exceed predictions based on body weights for either season, and resemble published data for another highly active mammalian group, the insectivorous shrews. Both tau ht and the minimal septal thickness of 0.083 micron approach the anatomical limits for thinning of alveolar septa without loss of epithelial continuity. Although both the heart and lungs lost 13% of their fresh weights during hibernation, compared to 25% for the liver, the lung contents of DNA (0.14 mg) and blood-free protein (7.38 mg) were not altered significantly. These small bats possess lungs which are well suited for the high aerobic cost of flight. Those lungs are resistant to hibernation-induced proteolysis, and also resistant to the deterioration of alveolar membranes which occurs in nonhibernators subjected to starvation-induced weight losses of similar magnitude.

Animals↗

Renal function in the neotropical bat, Artibeus jamaicensis.

1. When feeding on figs (Ficus insipida), the bat Artibeus jamaicensis increases dietary sodium density while decreasing potassium density by primarily extracting and ingesting pulp juices rather than other parts of the fruit. 2. Based on urine osmotic pressure, these bats are uniformly dehydrated when they leave day roosts and become rapidly rehydrated (0.5-1 hr) after initiation of feeding. 3. After 2000 hr, and throughout the night there is no difference in urine concentration of free-flying bats compared with bats held in the laboratory without food or water for the same time interval. 4. Mean maximum urine concentration in this species is 972 mOsm/kg.

Animals↗

Haematology and iron status of the Egyptian fruit bat, Rousettus aegyptiacus.

1. Haematological values and iron status of wild and captive fruit bats (Rousettus aegyptiacus) were determined. 2. Plasma iron concentrations were 175 micrograms/dl in wild males, and 286-316 micrograms/dl in captive bats. 3. Total splenic stores were small (around 100 micrograms) in relation to hepatic stores (3 mg) and total haem iron (2.6 mg). 4. Haemoglobin levels, red cell counts and haematocrits were unusually high and mean corpuscular volumes low. 5. Lactating wild bats showed no deficits in iron status or in haematological values. 6. It is concluded that the ascorbic acid content of fruit, together with the bats' high food requirement, has ensured an ample iron supply in this vegetarian species.

Animals↗

Temperature regulation in subtropical tree bats.

1. Rate of metabolism and temperature regulation were studied in five species of subtropical tree bats (Lasiurus seminolus, L. borealis, L. intermedius, L. cinereus and Nycticeius humeralis). 2. All species showed two states while resting below thermal neutrality: normothermia and torpor. Below 0-5 degrees C, bats in torpor maintained an intermediate body temperature. 3. Basal rate of metabolism was lower than expected on the basis of body mass (44-78%) and average body temperature in the normothermic state ranged between 32.5 and 35.7 degrees C. 4. Lasiurines have a high thermogenic capacity. 5. The metabolic and thermoregulatory traits studied in tree bats are generally similar to those of non-tropical bats roosting in caves and buildings.

Animals↗

Functional laminar and columnar organization of the auditory centers in echolocating Japanese greater horseshoe bats.

During echolocation, bats coordinately employ the vocalization system to emit orientation sounds and the auditory system to hear returning echoes. The brain in these animals should be functionally organized to process such biologically significant sounds. Here we utilized the autoradiographic 2-deoxy-[14C]glucose (DG) method to visualize functional organization of the auditory centers of echolocating Japanese greater horseshoe bats, Rhinolophus ferrumequinum nippon. Autoradiographic color images made from the brains of echolocating bats revealed a functional laminar structure in the inferior colliculus. Furthermore, a functional columnar organization appeared in the auditory cortex during echolocation. These laminar and columnar organization were not observed in the brain of resting bats.

Acoustic Stimulation↗

Tissue vitamin B12 levels in bat sucklings (Rousettus aegyptiacus) born of vitamin B12 deficient mothers.

The weights of the brains of vitamin B12-deficient baby bats (Rousettus aegyptiacus, 4-20 day old) were slightly lower than those of B12-replete infant bats. Liver and kidney organ weights were similar in the two groups. Brain and liver B12 levels of B12-deficient baby bats were significantly lower than those of replete controls. Kidney B12 levels in deficient babies were about one quarter those of the replete babies. Brain vitamin B12 levels in B12-deficient sucklings were significantly lower than those of B12-deficient adult bats (P less than 0.01). These findings reinforce the need for adequate vitamin B12 nutrition in pregnant and lactating animals.

Aging↗

Pinna position affects the auditory space representation in the inferior colliculus of the FM bat, Eptesicus fuscus.

Using free-field acoustic stimulus conditions, we studied the auditory space representation in the inferior colliculus (IC) of the big brown bat, Eptesicus fuscus, under different pinna positions. Stimuli were delivered from a loudspeaker placed 14 cm in front of the bat to determine the best frequency (BF) of an isolated neuron. A BF stimulus was then delivered as the loudspeaker was moved across the frontal auditory space of the bat to locate the response center of the neuron. At the response center, the neuron has its lowest minimum threshold (MT). The stimulus was then raised 5-dB above the lowest MT to measure the spatial response area. Both response center and spatial response area of each neuron were measured under different pinna positions. Variations in the response center and MT of each neuron under different pinna positions was determined and a possible reason for this variation was discussed. The variation in auditory space representation in the IC due to variation in pinna position is presented. We suggest that during echolocation a bat could make changes in its pinna position to create additional binaural disparity for accurate target localization.

Animals↗

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↗

Otoacoustic emissions from the cochlea of the 'constant frequency' bats, Pteronotus parnellii and Rhinolophus rouxi.

During stimulation with continuous pure tones, the cochlea of each individual of the mustached bat, Pteronotus parnellii, produces a strong evoked stimulus-frequency otoacoustic emission (SFOAE) at about 62 kHz. The SFOAEs were on average 480 Hz above the dominant constant frequency component of the echolocation call (resting frequency, RF). In two out of nine individuals of Pteronotus the SFOAEs changed into spontaneous otoacoustic emissions of 25-40 dB SPL. In the rufuous horseshoe bat, Rhinolophus rouxi spontaneous emissions were not detected and only in two out of seven animals were there weak SFOAEs about 300 Hz above the RF of 78 kHz. This difference may be due to a stronger damping of underlying resonant processes in Rhinolophus (Henson et al., 1985a). Acoustic distortion products behaved quite similar in both species. The first lower sideband distortion 2f1-f2 was measurable over a wide frequency range between 10 and 100 kHz. The optimum frequency separation delta f of the two primary tones to evoke maximum 2f1-f2 distortion was 0.8 to 5.8 kHz in Pteronotus and 1 to 7 kHz in Rhinolophus for frequencies outside the range of the constant frequency components of the call. This corresponds to ratios f2/f1 of about 1.03 to 1.2. At the frequency of the SFOAE in Pteronotus (480 Hz above the RF) and about 300 Hz above the RF in Rhinolophus the optimum delta f decreased sharply to values of 31-63 Hz in Pteronotus (ratio f2/f1 of 1.0005-1.001), and to 39-590 Hz in Rhinolophus (ratio f2/f1 of 1.0005-1.007). In Pteronotus a second minimum of delta f was found at about 90 kHz (values of 180-620 Hz, ratios f2/f1 of 1.002-1.007). In both bat species, the respective minima of delta f are located at or close to frequencies where neuronal tuning sharpness is exceptionally high. This indicates a mechanical origin of enhanced tuning. After adjusting the frequency of f2 to match the optimum delta fs, 2f1-f2 threshold curves were obtained. The distortion product threshold approximately parallels neuronal data and is in both species characterized by a pronounced insensitivity at the RF followed by a steep threshold minimum at frequencies 0.3-3 kHz above the RF. These features may be involved in reducing the cochlear response to the call such that the bats are able to focus on the Doppler-shifted echos which are slightly higher in frequency and thus within the range of the threshold minimum.

Acoustic Stimulation↗

Evidence of increased endometrial vascular permeability at the time of implantation in the short-nosed fruit bat, Cyanopterus sphinx.

Early embryonic development and implantation were studied in tropical short-nosed fruit bat Cyanopterus sphinx. We report preimplantation development and embryo implantation. Different stages of cleavage were observed in embryo by direct microscopic examination of fresh embryos after retrieving them either from the oviduct or the uterus at different days, up to the day of implantation. Generally, the embryos enter the uterus at the 8-cell stage. Embryonic development continued without any delay and blastocyst were formed showing attachment to the uterine epithelium at the mesometrial side of the uterus. A distinct blue band was formed in the uterus. The site of blastocyst attachment was visualized as a blue band following intravenous injection of pontamine blue. Implantation occurred 9+/-0.7 days after mating. This study reports that bat embryonic development can be studied like other laboratory animals and that this bat shows blue dye reaction, indicating the site and exact time of implantation. This blue dye reaction can be used to accurately find post-implantational delay. We prove conclusively that this species of tropical bat does not have any type of embryonic diapause.

Animals↗

A neural mechanism for detecting the distance of a selected target by modulating the FM sweep rate of biosonar in echolocation of bat.

Most species of bats making echolocation use frequency modulated (FM) ultrasonic pulses to measure the distance to targets. These bats detect with a high accuracy the arrival time differences between emitted pulses and their echoes generated by targets. In order to clarify the neural mechanism for echolocation, we present neural model of inferior colliculus (IC), medial geniculate body (MGB) and auditory cortex (AC) along which information of echo delay times is processed. The bats increase the downward frequency sweep rate of emitted FM pulse as they approach the target. The functional role of this modulation of sweep rate is not yet clear. In order to investigate the role, we calculated the response properties of our models of IC, MGB, and AC changing the target distance and the sweep rate. We found based on the simulations that the distance of a target in various ranges may be encoded the most clearly into the activity pattern of delay time map network in AC, when the sweep rate of FM pulse used is coincided with the observed value which the bats adopt for each range of target distance.

Animals↗

Annual reproductive synchronization in ovary and pineal gland function of female short-nosed fruit bat, Cynopterus sphinx.

We studied the annual correlation of ovarian activity and pineal gland in relation with seasonal variation and gestation of a tropical zone short-nosed fruit bat Cynopterus sphinx. Female bats showed bimodal polyestry (February/March and September/October) in their reproductive cycle. Plasma estradiol concentration ran parallel with ovarian activity and had an inverse relation with pineal mass and peripheral melatonin concentration. Due to the delayed embryonic development in the uterus (October-March) of female bats, interestingly, the uterine activity did not show a parallel relation with ovarian activity and estradiol level. Further, compared with normal non-pregnant females, melatonin level was high during gestation and delayed embryonic development phase. This suggests that the reproductive synchrony and annual variation in ovarian activity of this nocturnal flying mammal differ from other common tropical mammals. The delayed embryonic development in bats might be an adaptive strategy for the unfavorable conditions of the seasons and might be regulated by high peripheral estradiol and melatonin concentration.

Acclimatization↗

Cloning and expression of PDK4, FOXO1A and DYRK1A from the hibernating greater horseshoe bat (Rhinolophus ferrumequinum).

Pyruvate dehydrogenase kinase isoenzyme 4 (PDK4) cDNA was cloned from the brain of greater horseshoe bat (Rhinolophus ferrumequinum). The deduced amino acid sequence shares strong homology with these PDK4 of other mammals. Moreover, we partially cloned homologues of dual-specificity tyrosine-phosphorylated and regulated protein kinase 1A (DYRK1A), and forkhead box protein O1A (FOXO1A) from greater horseshoe bat. Among five different tissues tested, PDK4 mRNA was highly expressed in the heart, white adipose tissue and muscle, but weakly expressed in the brain and liver, while DYRK1A and FOXO1A were expressed in all five tissues. Moreover, the transcript levels of PDK4, DYRK1A, and FOXO1A were measured in the heart, white adipose tissue and muscle of hibernating and arousal greater horseshoe bats by Northern blot and real time PCR. The results showed that transcript level of PDK4 was significantly higher in white adipose tissue. Expression level of DYRK1A was significantly higher in hibernating state in white adipose tissue, and expression level of FOXO1A was significantly higher in muscle in aroused state. These results suggest that up-regulation of the transcript levels of PDK4 during hibernation were not regulated via DYRK1A and FOXO1A in white adipose tissue and muscle, and the possible presence of another isoenzyme of PDK which is responsible for the tissue-specific regulation of Pyruvate dehydrogenase complex (PDC) activity in the bat heart during hibernation.

Animals↗

Effects of short-term fasting on energy reserves of vampire bats (Desmodus rotundus).

Studies on metabolic responses to fasting in common vampire bats (Desmodus rotundus) have demonstrated the susceptibility of this species when subjected to long-term fasting. We investigated the effects of short-term fasting (12 h), a period similar to what they face in the field, on their energy reserves. Blood glucose (BG) levels in fed bats were similar to other mammals, but after 12 h without food, these levels were reduced. Plasma lactate and free fatty acids levels in fed bats were higher than in other mammals, although no changes in these levels were detected in response to fasting. Liver glycogen content decreased significantly following fasting. Muscle glycogen, as well as liver and muscle lipid and protein levels, remained unaltered for up to 12 h of fasting. Although BG levels decreased after short-term fasting, body energy reserves do not seem to play an important role for maintenance of glycemic homeostasis during fasting. Despite the decrease in liver glycogen, this small reserve seems insufficient to maintain adequate levels of BG, even during short periods of fasting. Because other reserves were not decreased after fasting, it is possible that the main source of glucose for common vampire bats might be the glucose content of their blood diet.

Animals↗

Directionality of hearing in two CF/FM bats, Pteronotus parnellii and Rhinolophus rouxi.

The head-related transfer function (HRTF) has been measured in two CF/FM bats, Pteronotus parnellii and Rhinolophus rouxi from 575 positions in the frontal hemisphere. P. parnellii showed an increase of the elevation angle of the axis of highest pinna gain with increasing frequency followed by a specific decrease at 75 kHz. Such a drop of elevation angle of the acoustic axis was not seen in R. rouxi. The HRTF further showed a spectral notch dependent on elevation and frequency in P. parnellii, but not in R. rouxi. The functional implications of this difference between both bat species are discussed. Frequencies at maximum pinna gain values did not clearly match the frequencies of the harmonics of the echolocation calls whereas spatial resolution of interaural intensity differences was best in a frequency range that included the higher harmonics of the echolocation calls in both bat species. However, specializations of HRTF patterns matching the exact frequencies of the harmonics of the echolocation calls could not be observed in both bat species.

Acoustic Stimulation↗

Batting with occluded vision: an in situ examination of the information pick-up and interceptive skills of high- and low-skilled cricket batsmen.

The capability of cricket batsmen of different skill levels to pick-up information from the pre-release movement pattern of the bowler, from pre-bounce ball flight, and from post-bounce ball flight was examined experimentally. Six highly skilled and six low-skilled cricket batsmen batted against three different leg-spin bowlers while wearing liquid crystal spectacles. The spectacles permitted the specific information available to the batsmen on each trial to be manipulated such that vision was either: (i) occluded at a point prior to the point of ball release (thereby only allowing vision of advance information from the bowler's delivery action); (ii) occluded at a point prior to the point of ball bounce (thereby permitting the additional vision of pre-bounce ball flight); or (iii) not occluded (thereby permitting the additional vision of post-bounce ball flight information). Measurement was made on each trial of both the accuracy of the definitive (forward-backward) foot movements made by the batsmen and their success (or otherwise) in making bat-ball contact. The analyses revealed a superior capability of the more skilled players to make use of earlier (pre-bounce) ball flight information to guide successful bat-ball interception, thus mirroring the greater use of prospective information pick-up by skilled performers observed in other aspects of batting and in other time-constrained performance domains.

Humans↗

Reduced free-radical production and extreme longevity in the little brown bat (Myotis lucifugus) versus two non-flying mammals.

The extended longevity of bats, despite their high metabolic rate, may provide insight to patterns and mechanisms of aging. Here I test predictions of the free radical or oxidative stress theory of aging as an explanation for differences in lifespan between the little brown bat, Myotis lucifugus (maximum lifespan potential MLSP=34 years), the short-tailed shrew, Blarina brevicauda (MLSP=2 years), and the white-footed mouse, Peromyscus leucopus (MLSP=8 years) by comparing whole-organism oxygen consumption, hydrogen peroxide production, and superoxide dismutase activity in heart, kidney, and brain tissue. Mitochondria from M. lucifugus produced half to one-third the amount of hydrogen peroxide per unit of oxygen consumed compared to mitochondria from B. brevicauda and P. leucopus, respectively. Superoxide dismutase (SOD) activity did not differ among the three species. These results are similar to those found for birds, which like bats have high metabolic rates and extended longevities, and provide support for the free radical theory of aging as an at least partial explanation for the extreme longevity of bats.

Animals↗