Frequency and space representation in the inferior colliculus of the FM bat,Eptesicus fuscus

Summary The tonotopic organization and spatial sensitivity of 217 inferior collicular (IC) neurons of Eptesicus fuscus were studied under free field stimulation conditions. Acoustic stimuli were delivered from a loudspeaker placed 21 cm ahead of the bat to determine the best frequency (BF) and minimum threshold (MT) of isolated IC neurons. A BF stimulus was then delivered as the loudspeaker was moved horizontally across the frontal auditory space of the bat to locate the best azimuthal angle (BAZ) at which the neuron had its lowest MT. The stimulus was then raised 3 dB above the lowest MT to determine the horizontal extent of the auditory space within which a sound could elicit responses from the neuron. This was done by moving the loudspeaker laterally at every 5° or 10° until the neuron failed to respond. These measurements also allowed us to redetermine the BAZ at which the neuron fired maximal number of impulses. Electrodes were placed evenly across the whole IC surface and IC neurons were sampled as many as possible within each electrode penetration. Tonotopic organization and spatial sensitivity were examined among all 217 IC neurons as a whole as well as among IC neurons sequentially sampled within individual electrode penetrations. The whole population of 217 IC neurons is organized tonotopically along the dorsoventral axis of the IC. Thus, low frequency neurons are mostly located dorsally and high frequency neurons ventrally with median frequency neurons intervening in between. The BAZ of these 217 IC neurons tend to shift from lateral to medial portions of the contralateral frontal auditory space with increasing BF. Thus, the auditory space appears to have an orderly representation along the tonotopic axis of the IC. The lateral space is represented dorsally and the medial space ventrally. Nevertheless, tonotopic organization and spatial sensitivitty of sequentially isolated IC neurons within each electrode penetration may vary with the point of electrode penetration. This variation may be explained on the basis of the arrangement and thickness of each frequency lamina within the IC.     

Retinofugal projections of the big brown bat,Eptesicus fuscus and the neotropical fruit bat,Artibeus jamaicensis

Retinal connections were studied in Eptesicus fuscus and Artibeus jamaicensis using anterograde axonal degeneration and autoradiographic techniques following unilateral enucleations and uniocular injections of radioactive amino acids. Although each retina projected bilaterally to the brainstem, the number of silver grains in the emulsion of autoradiographs indicated that nearly all fibers in the optic nerve entered the contralateral optic tract. Ipsilaterally, a major portin of the projection ended in the suprachiasmatic nucleus; caudal to the suprachiasmatic nucleus, the amount of label was so small that individual silver grains were counted to determine the location and quantity of lebel in other ipsilateral nuclei. In both species the retinal projection terminated bilaterally in the suprachiasmatic, dorsal lateral geniculate, ventral lateral geniculate, and pretectal olivary nuclei and contralaterally in the posterior pretectal nucleus, superficial gray layers of the superior colliculus, and nuclei of the accessory optic system. In Eptesicus the projection to the nucleus of the optic tract ended contralaterally, and in Artibeus it ended in this nucleus bilaterally. The results of this study revealed a basic theme in the optic projection of the two ecologically different microchirop. terans. The results differed, however, in that the projection was larger and visually related nuclei were better developed in Artibeus. Such variations are presumed to relate to eye size and the relative use of vision by the two chiropterans.     

An electrophysiological study of neural pathways for corticofugally inhibited neurons in the central nucleus of the inferior colliculus of the big brown bat, Eptesicus fuscus

This electrophysiological study tests the hypothesis that one possible neural pathway for corticofugally inhibited neurons in the central nucleus of the inferior colliculus (ICc) of the big brown bat, Eptesicus fuscus, is mediated through excitatory projections from the auditory cortex (AC) to the external nucleus of the IC (ICx), which then sends inhibitory inputs to the ICc. This study shows that all neurons in the ICx are broadly tuned to stimulus frequency. Electrical stimulation in the AC typically increases the number of impulses, expands the auditory spatial response areas, and broadens the frequency tuning curves (FTCs) of neurons in the ICx. This corticofugal facilitation is mediated at least in part through NMDA receptors, since application of DL-2-amino-5-phosphonovaleric acid (APV), an antagonist for NMDA, decreases these response properties of neurons in the ICx. Electrical stimulation in the ICx typically decreases the number of impulses, reduces the auditory spatial response areas, and narrows the FTCs of neurons in the ICc. This inhibition is mediated at least in part through GABA_A receptors, since application of bicuculline, an antagonist for GABA, increases these response properties of neurons in the ICc. These data suggest that corticofugal facilitation of the ICx and the inhibition of the ICx to the ICc may be one of the polysynaptic pathways for corticofugal inhibition of neurons in the ICc. Possible functions of this polysynaptic pathway in acoustic orientation and signal processing are discussed. Electronic Publication     

Echo frequency selectivity of duration-tuned inferior collicular neurons of the big brown bat, Eptesicus fuscus, determined with pulse-echo pairs

During hunting, insectivorous bats such as Eptesicus fuscus progressively vary the repetition rate, duration, frequency and amplitude of emitted pulses such that analysis of an echo parameter by bats would be inevitably affected by other co-varying echo parameters. The present study is to determine the variation of echo frequency selectivity of duration-tuned inferior collicular neurons during different phases of hunting using pulse-echo (P-E) pairs as stimuli. All collicular neurons discharge maximally to a tone at a particular frequency which is defined as the best frequency (BF). Most collicular neurons also discharge maximally to a BF pulse at a particular duration which is defined as the best duration (BD). A family of echo iso-level frequency tuning curves (iso-level FTC) of these duration-tuned collicular neurons is measured with the number of impulses in response to the echo pulse at selected frequencies when the P-E pairs are presented at varied P-E duration and gap. Our data show that these duration-tuned collicular neurons have narrower echo iso-level FTC when measured with BD than with non-BD echo pulses. Also, IC neurons with low BF and short BD have narrower echo iso-level FTC than IC neurons with high BF and long BD have. The bandwidth of echo iso-level FTC significantly decreases with shortening of P-E duration and P-E gap. These data suggest that duration-tuned collicular neurons not only can facilitate bat's echo recognition but also can enhance echo frequency selectivity for prey feature analysis throughout a target approaching sequence during hunting. These data also support previous behavior studies showing that bats prepare their auditory system to analyze expected returning echoes within a time window to extract target features after pulse emission.     

Brief and short-term corticofugal modulation of subcortical auditory responses in the big brown bat, Eptesicus fuscus

Recent studies show that the auditory corticofugal system modulates and improves ongoing signal processing and reorganizes frequency map according to auditory experience in the central nucleus of bat inferior colliculus. However, whether all corticofugally affected collicular neurons are involved in both types of modulation has not been determined. In this study, we demonstrate that one group (51%) of collicular neurons participates only in corticofugal modulation of ongoing signal processing, while a second group (49%) of collicular neurons participates in both modulation of ongoing signal processing and in reorganization of the auditory system.     

Unique characteristics of bat rabies viruses in big brown bats (Eptesicus fuscus)

Rabies virus infection has been documented in several North American bat species, including Eptesicus fuscus. The virus-host relationship between bats and rabies virus (RV) is not well understood. The incidence of non-lethal RV exposure, based on the presence of viral neutralizing antibodies, demonstrates that exposure to RV does not always lead to clinical infection in bats. It is unknown how the route of exposure, rabies virus variant, or health of the bat affects the outcome following exposure. This paper describes the pathogenesis of two big brown bat RV variants in homologous host species. Our study demonstrates that RV variants obtained from the same species of bat from similar geographical areas may result in a diverse clinical progression of disease.     

Selectivity for echo spectral interference and delay in the auditory cortex of the big brown bat Eptesicus fuscus

The acoustic environment for an echolocating bat can contain multiple objects that reflect echoes so closely separated in time that they are almost completely overlapping. This results in a single echo with a spectrum characterized by deep notches due to interference. The object of this study was to document the possible selectivity, or lack thereof, of auditory neurons to the temporal separation of biosonar signals on a coarse (ms) and fine (micros) temporal scale. We recorded single-unit activity from the auditory cortex of big brown bats while presenting four protocol designs using wideband FM signals. The protocols simulated a pair of partially overlapping echoes where the separation between the first and second echo varied between 0 and 72 micros, a pulse followed by a single echo at varying delay from 0 to 30 ms, a pulse followed at a fixed delay by a pair of partially overlapping echoes that had a varying temporal separation of 0-72 micros, and a pulse followed, with a varying delay between 0 and 30 ms, by a pair of echoes that themselves had a fixed temporal separation on a microsecond time scale. About half of the cortical units showed increased spike counts to pairs of partially overlapping echoes at particular separations (6-72 micros) compared with a baseline stimulus at 0-micros separation. For many neurons tested with a pulse followed by two overlapping echoes, we observed a sensitivity to the coarse delay between the pulse and pair of overlapping echoes and to the separation between the two echoes themselves. The sensitivity to the partial overlap between the two echoes was not tuned to a single temporal separation. For bats, this means that the absolute range to the closest reflector and range between reflectors may be jointly encoded across a small population of single units. There are several possible neuronal mechanisms for encoding the separation between two nearby echoes based on the sensitivity to spectral notches.     

An analysis of correspondence between unique rabies virus variants and divergent big brown bat (Eptesicus fuscus) mitochondrial DNA lineages

The literature supports that unique rabies virus (RABV) variants are often compartmentalized in different species of bats. In Colorado, two divergent mtDNA lineages of big brown bats (Eptesicus fuscus) co-occur. RABV associated with this species also segregates into two clades. We hypothesized that unique RABV variants might be associated with mtDNA lineages of Colorado big brown bats. DNA was extracted from brain tissue of rabid big brown bats, the ND2 gene was amplified to determine mtDNA lineage, and the lineage was compared to a previously derived phylogenetic analysis of the RABV N gene. No correspondence was found between host bat lineage and RABV variant.     

Experimental infection of big brown bats (Eptesicus fuscus) with Eurasian bat lyssaviruses Aravan, Khujand, and Irkut virus

Summary. Here we describe the results of experimental infections of captive big brown bats (Eptesicus fuscus) with three newly isolated bat lyssaviruses from Eurasia (Aravan, Khujand, and Irkut viruses). Infection of E. fuscus was moderate (total, 55–75%). There was no evidence of transmission to in-contact cage mates. Incubation periods for Irkut virus infection were significantly shorter (p < 0.05) than for either Aravan or Khujand virus infections. In turn, quantification of viral RNA by TaqMan PCR suggests that the dynamics of Irkut virus infection may differ from those of Aravan/Khujand virus infection. Although infectious virus and viral RNA were detected in the brain of every rabid animal, dissemination to non-neuronal tissues was limited. Levels of viral RNA in brain of Aravan/Khujand virus-infected bats was significantly correlated with the number of other tissues positive by TaqMan PCR (p < 0.05), whereas no such relationship was observed for Irkut virus infection (where viral RNA was consistently detected in all tissues other than kidney). Infectious virus was isolated sporadically from salivary glands, and both infectious virus and viral RNA were obtained from oral swabs. The detection of viral RNA in oral swabs suggests that viral shedding in saliva occurred <5 days before the onset of clinical disease.     

Observations on the pineal gland of the big brown bat,Eptesicus fuscus: Possible correlation of melanin intensification with constant darkness

Background: Our initial observation of the macroscopically pigmented pineal gland of the big brown bat, Eptesicus fuscus, led to this study. Information has been lacking on pigmentation in the pineal and its significance in mammals in general and bats in particular. This report begins to address this situation. Methods: Bats were examined both in the wild and after exposure to various experimental conditions. The pineals were examined macroscopically as well as with light and electron microscopy. The pigment was identified as melanin by its color, the ultrastructure of its granules, and their reaction with hydrogen peroxide. Results: Gross observations showed the pineals to be variably pigmented, which were subjectively scored from unpigmented to heavily pigmented. Pineals from bats exposed to a continuous 24 h light regimen or those from a summer population contained very little, if any, externally visible melanin. Such pineals are considered unpigmented in this study. In contrast, pineals from 74% of 156 animals taken together, either subjected to constant darkness or hibernation (simulated or natural), exhibited very heavily pigmented pineals. The pigment in these cases even extended to the juxtapineal meningeal covering. The pineal was pigmented even in a newborn Eptesicus. Conclusions: The pineal pigmentation in the big brown bat appears to intensify with constant darkness and may vary seasonally. The observation of macroscopically pigmented pineals in some other bats (Myotis lucifugus, Pipistrellus subfiavus, and Lasiurus borealis) suggests that this phenomenon may be of taxonomic value for the family Vespertilionidae (Order Chiroptera). © 1994 Wiley-Liss, Inc.     

Response properties and location of neurons selective for sinusoidal frequency modulations in the inferior colliculus of the big brown bat

Most animal vocalizations, including echolocation signals used by bats, contain frequency-modulated (FM) components. Previous studies have described a class of neurons in the inferior colliculus (IC) of the big brown bat that respond exclusively to sinusoidally frequency modulated (SFM) signals and fail to respond to pure tones, noise, amplitude-modulated tones, or single FM sweeps. The aims of this study were to further characterize these neurons' response properties and to determine whether they are localized within a specific area of the IC. We recorded extracellularly from 214 neurons throughout the IC. Of these, 47 (22%) responded exclusively to SFM. SFM-selective cells were tuned to relatively low carrier frequencies (9-50 kHz), low modulation rates (20-210 Hz), and shallow modulation depths (3-10 kHz). Most had extremely low thresholds, with an average of 16.5 +/- 7.6 dB SPL, and 89% had upper thresholds and closed response areas. For SFM-selective cells with spontaneous activity, the spontaneous activity was eliminated when sound amplitude exceeded their upper threshold and resumed after the stimulus was over. These findings suggest that SFM-selective cells receive low-threshold excitatory inputs and high-threshold inhibitory inputs. SFM-selective cells were clustered in the rostrodorsal part of the IC. Within this area, best modulation rate appeared to be correlated with best carrier frequency and depth within the IC.     

Duration selectivity of neurons in the inferior colliculus of the big brown bat: tolerance to changes in sound level

At and above the level of the inferior colliculus (IC), some neurons respond maximally to a limited range of sound durations, with little or no excitatory response to durations outside of this range. Such neurons have been termed "duration tuned" or "duration selective." In this study we examined the effects of varying signal amplitude on best duration, width of tuning, and first spike latency of duration tuned neurons in the IC of the big brown bat, Eptesicus fuscus. Response areas as a function of stimulus duration and intensity took a variety of forms, including open (V-shaped), narrow and level tolerant (U-shaped), or closed (O-shaped). The majority (82%) of duration tuned neurons had narrow U-shaped or O-shaped duration response areas. Those with narrow U-shaped response areas retained their duration tuning across a broad dynamic range, < or = 50 dB above threshold, whereas those with O-shaped response areas were narrowly tuned to both stimulus duration and amplitude. For about one-half (55%) of the neurons with either a U- or O-shaped response areas, best duration (BD) changed by <1 ms across the range of suprathreshold amplitudes tested. Changes in BD most often took the form of a shift to slightly shorter durations as stimulus level increased. For the majority (65%) of U- and O-shaped neurons, 50% width of duration tuning changed by <2 ms with increasing amplitude. Latency of response at BD remained stable across changes in sound level, suggesting that the relative strengths of excitatory and inhibitory inputs to duration tuned neurons remain in balance over a wide dynamic range of sound pressure levels.     

Determinants of horizontal sound location selectivity of binaurally excited neurons in an isofrequency region of the mustache bat inferior colliculus

1. The monaural and binaural response properties and the horizontal sound location sensitivity of 78 binaurally excited neurons from 26 bats were examined with a combined closed-field and free-field stimulation paradigm. The aim was to determine how the response properties of these neurons shape their selectivity for auditory space. All neurons were recorded within a single, greatly enlarged isofrequency (60 kHz) region of the mustache bat's central nucleus of the inferior colliculus (ICC). In this and two companion papers (Wenstrup et al. 1988a,b) that focused on binaurally inhibited neurons in this isofrequency region, our goal was to examine the neural mechanisms for binaural processing within a single frequency channel of the primary auditory system. 2. Binaurally excited neurons were defined as either excited by monaural input from both ears or, if excited by monaural stimulation of only one ear, facilitated by binaural stimulation. Some neurons also exhibited binaural inhibition. These neurons were divided into functional classes based on their responses to monaural and binaural stimulation presented under dichotic, closed-field conditions. The following notation was used: response to contralateral stimulation (E, excitatory; O, no effect), response to ipsilateral stimulation (E, excitatory; O, no effect)/response to binaural stimulation (F, facilitatory; I, inhibitory; O, no effect). Seven functional classes were observed: EE/O, EE/F, EE/I, EE/FI, EO/F, EO/FI, and OO/F. 3. Among EE neurons, thresholds for contralateral monaural stimulation were typically lower than for ipsilateral stimulation, and response magnitudes for contralateral stimulation were typically greater. Among EO/F and EO/FI neurons, only one eye, an OE/FI neuron, was excited by ipsilateral monaural stimulation. These results suggest that contralateral input provides the dominant excitatory influence. EE/FI and EO/FI neurons, which exhibited both binaural facilitation and inhibition, were typically inhibited at interaural intensity differences (IIDs) favoring the ipsilateral ear, suggesting that ipsilateral input provides the dominant inhibitory influence. 4. Neurons were tested over the range of naturally occurring IIDs (+/- 30 dB) at intensities of -20 to 30 dB relative to threshold. The IID functions of these neurons assumed three configurations: flat, with facilitation occurring at all IIDs; stepped, with facilitation occurring over part of the IID range, and peaked, with facilitation occurring over a limited band of IIDs. The majority of cells (90%) exhibited peaked IID functions, and most of these (73%), regardless of functional class, were maximally facilitated at an IID of 0 dB. 5. Neurons differed considerably in the strength of their binaural interactions.(ABSTRACT TRUNCATED AT 400 WORDS)     

Duration tuning in the inferior colliculus of the mustached bat

We studied duration tuning in neurons of the inferior colliculus (IC) of the mustached bat. Duration-tuned neurons in the IC of the mustached bat fall into three main types: short (16 of 136), band (34 of 136), and long (29 of 136) pass. The remaining 51 neurons showed no selectivity for the duration of sounds. The distribution of best durations was double peaked with maxima around 3 and 17 ms, which correlate with the duration of the short frequency-modulated (FM) and the long constant-frequency (CF) signals emitted by Pteronotus parnellii. Since there are no individual neurons with a double-peaked duration response profile, both types of temporal processing seem to be well segregated in the IC. Most short- and band-pass units with best frequency in the CF2 range responded to best durations > 9 ms (66%, 18 of 27 units). However, there is no evidence for a bias toward longer durations as there is for neurons tuned to the frequency range of the FM component of the third harmonic, where 83% (10 of 12 neurons) showed best durations longer than 9 ms. In most duration-tuned neurons, response areas as a function of stimulus duration and intensity showed either V or U shape, with duration tuning retained across the range of sound levels tested. Duration tuning was affected by changes in sound pressure level in only six neurons. In all duration-tuned neurons, latencies measured at the best duration were longer than best durations, suggesting that behavioral decisions based on analysis of the duration of the pulses would not be expected to be complete until well after the stimulus has occurred.     

Iso-frequency 2-DG contours in the inferior colliculus of the awake monkey

Summary Tone bursts produced bands of selective 2-[¹⁴C]-deoxyglucose labelling in the inferior colliculus (IC) of the awake monkey. Low tone frequencies produced labelling in dorsal regions and high tone frequencies produced labelling in ventral regions. The position of the bands coincided with the position of a single unit with a characteristic frequency, which was the same as the frequency producing the labelling. These findings indicate that the bands of labelling represent iso-frequency contours in IC. The iso-frequency contours extended across most of the nucleus and were oriented from dorsomedially to ventro-laterally at 20–30° from the horizontal and became more vertical anteriorly. The width of the contours was as narrow as 200 m, suggesting that the contours might represent 2 or 3 overlapping cellular laminae.Supported by research grants from the National Health and Medical Research Council of Australia and the Australian Research Grants Scheme