Marianne Vater

The functional role of GABA and glycine in monaural and binaural processing in the inferior colliculus of horseshoe bats

SummaryThe functional role of GABA and glycine in monaural and binaural signal analysis was studied in single unit recordings from the central nucleus of the inferior colliculus (IC) of horseshoe bats (Rhinolophus rouxi) employing microiontophoresis of the putative neurotransmitters and their antagonists bicuculline and strychnine.Most neurons were inhibited by GABA (98%; N=107) and glycine (92%; N=118). Both neurotransmitters appear involved in several functional contexts, but to different degrees.Bicuculline-induced increases of discharge activity (99% of cells; N=191) were accompanied by changes of temporal response patterns in 35% of neurons distributed throughout the IC. Strychnine enhanced activity in only 53% of neurons (N=147); cells exhibiting response pattern changes were rare (9%) and confined to greater recording depths. In individual cells, the effects of both antagonists could markedly differ, suggesting a differential supply by GABAergic and glycinergic networks.Bicuculline changed the shape of the excitatory tuning curve by antagonizing lateral inhibition at neighboring frequencies and/or inhibition at high stimulation levels. Such effects were rarely observed with strychnine.Binaural response properties of single units were influenced either by antagonization of inhibition mediated by ipsilateral stimulation (bicuculline) or by changing the strength of the main excitatory input (bicuculline and strychnine).

The cochlear frequency map of the mustache bat, Pteronotus parnellii.

SummaryThe frequency-place map of the cochlea of mustache bats was constructed by the analysis of HRP-transport patterns in spiral ganglion cells following iontophoretic tracer injections into cochlear nucleus regions responsive to different frequencies.The cochlea consists of 5 half turns (total length 14.3 mm) and the representation of certain frequency bands can be assigned to specific cochlear regions:1.The broad high frequency range between 70 and 111 kHz is represented in the most basal half turn within only 3.2 mm. This region is terminated apically by a distinct narrowing of the scala vestibuli that coincides with a pronounced increase in basilar membrane (BM) thickness.2.The narrow intermediate frequency range between 54 and 70 kHz is expanded onto 50% of cochlear length between 4.0 and 11.1 mm distance from apex. The frequency range around 60 kHz, where the tuning characteristics of the auditory system are exceptionally sharp, is located in the center of this expanded BM-region in the second half turn within a maximum of innervation density. These data can account for the vast overrepresentation of neurons sharply tuned to about 60 kHz at central stations of the auditory pathway. In the cochlear region just basal to the innervation maximum, where label from injections at 66 and 70 kHz was found, a number of morphological specializations coincide: the BM is maximally thickened, innervation density is low, the spiral ligament is locally enlarged, and the ‘thick lining’, a dense covering of the scala tympani throughout the basal halfturn, suddenly disappears.3.Low frequencies up to 54 kHz are represented within the apical half turns over a 4 mm span of the basilar membrane. The data are compared to the cochlea of horseshoe bats and the possible functional role of the morphological discontinuities for sharp tuning and the generation of otoacoustic emissions is discussed.

The columnar region of the ventral nucleus of the lateral lemniscus in the big brown bat (Eptesicus fuscus): synaptic arrangements and structural correlates of feedforward inhibitory function

Abstract.Neurons of the columnar region of the ventral nucleus of the lateral lemniscus of Eptesicus fuscus respond with high-precision constant-latency responses to sound onsets and possess remarkably broad tuning. To study the synaptic basis for this specialized monaural auditory processing and to elucidate the excitatory or inhibitory nature of the input and output circuitry, we have used classical transmission electron microscopy, and postembedding immunocytochemistry for gamma aminobutyric acid (GABA) and glycine on serial semithin sections. The dominant putatively excitatory perisomatic input is provided by large calyx-like terminals that possess round synaptic vesicles and asymmetric synaptic contacts. Additionally, calyces contact the dendrites of neighboring neurons. Putatively inhibitory small boutons possess pleomorphic or flattened synaptic vesicles and symmetrical contacts and are sparsely distributed on somata and dendrites. Almost all neurons are glycine-immunoreactive. There is a moderate amount of glycine-immunoreactive puncta; GABA-immunoreactive puncta are rare. This suggests that (1) there is a fast robust excitatory synaptic input via calyx-like perisomatic endings, (2) calyx-like endings distribute frequency-specific excitatory input across isofrequency sheets by virtue of parallel synapses to somata and adjacent dendrites, and thus, dendritic integration may contribute to the broadening of frequency tuning, (3) the columnar region forms an inhibitory glycinergic feedforward relay in the ascending auditory pathway, a relay that is probably involved in creating filters for time-varying signals.

Evoked acoustic emissions and cochlear microphonics in the mustache bat, Pteronotus parnellii.

In the echolocating bat, Pteronotus parnellii, otoacoustic responses at a frequency of 62 kHz are measurable in the external ear canal during continuous and after transient acoustic stimulation. These responses are interpreted to represent emissions from the cochlea. They can reach an amplitude as large as 70 dB SPL and occur in the frequency range most important for echolocation, namely on the average about 700 Hz above the constant frequency component of the orientation calls. A sharp maximum of the amplitude of cochlear microphonic potentials at about 62 kHz could be correlated with the emission frequency. In one bat an evoked otoacoustic response changed to a spontaneous otoacoustic emission. The frequency and amplitude of the evoked otoacoustic responses reversibly decreased after exposure for 1 min to continuous sounds of more than 85 dB SPL with frequencies of about 2.5-7.5 kHz above the emission frequency. Similar effects occurred during anaesthesia or cooling. A possible relation between the existence of otoacoustic emissions and morphological specializations of the cochlea is discussed.

Comparative aspects of cochlear functional organization in mammals.

This review addresses the functional organization of the mammalian cochlea under a comparative and evolutionary perspective. A comparison of the monotreme cochlea with that of marsupial and placental mammals highlights important evolutionary steps towards a hearing organ dedicated to process higher frequencies and a larger frequency range than found in non-mammalian vertebrates. Among placental mammals, there are numerous cochlear specializations which relate to hearing range in adaptation to specific habitats that are superimposed on a common basic design. These are illustrated by examples of specialist ears which evolved excellent high frequency hearing and echolocation (bats and dolphins) and by the example of subterranean rodents with ears devoted to processing low frequencies. Furthermore, structural functional correlations important for tonotopic cochlear organization and predictions of hearing capabilities are discussed.

Cochlear Structure and Function in Bats

The mammalian cochlea must extract loudness and frequency information about different and overlapping acoustic events from a single input channel. Unlike the visual system, where input from different spatial sources is separated early and distributed in parallel channels, all input to the cochlea converges in the middle ear to induce movement at the membrane of the oval window. The oval window acts as a point source of mechanical waves dissipating in the fluid-filled spaces of the cochlea. It is now left to the organ of Corti to filter relevant information from the total input. Because this is a difficult task, it is no wonder that the acquisition of highly developed cochleae that are able to analyze low-level signals at many different frequencies is a relatively recent step in animal evolution, one that is confined to higher vertebrates. The high-frequency hearing capabilities of reptiles and birds are restricted to frequencies below about 12 kHz (for review, see Manley 1990). As a specific mammalian adaptation, the middle ear and the cochlea have an extended sensitivity in the high-frequency range. For processing of high frequencies, the cochlea has developed macro- and micromechanical specializations and employs active processes that enhance frequency tuning and sensitivity.

Resonance phenomena in the cochlea of the mustache bat and their contribution to neuronal response characteristics in the cochlear nucleus

SummaryThe cochlea of the mustache bat, Pteronotus parnellii, is very sensitive and sharply tuned to the frequency range of the dominant second harmonic of the echolocation call around 61 kHz. About 900 Hz above this frequency the cochlear microphonic potential (CM) reaches its maximum amplitude and lowest threshold. At exactly the same frequency, pronounced evoked otoacoustic emissions (OAE) can be measured in the outer ear canal, indicating mechanical resonance. The CM amplitude maximum and the OAE are most severely masked by simultaneous exposure to tones within the range from about 61–62 kHz up to about 70 kHz. The data suggest that the mechanism of mechanical resonance involves cochlear loci basal to the 61 kHz position.The resonance contributes to auditory sensitivity and sharp tuning: At the frequency of the OAE, single unit responses in the cochlear nucleus have the lowest thresholds. Maximum tuning sharpness occurs at frequencies about 300 Hz below the OAE-frequency, where the threshold is about 10 dB less sensitive than at the OAE-frequency. In addition, in the frequency range around the OAE-frequency several specialized neuronal response features can be related to mechanical resonance: Long lasting excitation after the end of the stimulus, asymmetrical tuning curves with a shallow high frequency slope and phasic ‘on-off’ neuronal response patterns. In particular the latter phenomenon indicates the occurrence of local mechanical cancellations in the cochlea.

A microiontophoretic study of acetylcholine effects in the inferior colliculus of horseshoe bats: implications for a modulatory role.

The effects of acetylcholine (ACh) in processing acoustical information in the inferior colliculus (IC) of awake horseshoe bats (Rhinolophus rouxi) were examined with single cell recordings and microiontophoresis. Cholinergic agonists, acetylcholine and carbachol raised the stimulus evoked discharge in 37% and suppressed responses in 16% of the sample. They did not alter the shapes of tuning curves and rate-intensity functions but the latter showed parallel shifting. The nicotinic antagonist, hexamethonium raised neuronal activity in 52% of neurons without affecting discharge patterns. The nonspecific muscarinic antagonist atropine was mostly inhibitory (62% of units) and caused changes in temporal discharge patterns by affecting the tonic response component. The selective muscarinic ml antagonist pirenzepine, also had an inhibitory effect (37% of units) and predominantly influenced the tonic response component. The selective m2 antagonist, gallamine however produced mainly excitatory effects (64% of units) and changed temporal discharge patterns by adding tonic response components. These findings may indicate a differential pre- and postsynaptic synaptic distribution of m1/m2 receptors in the inferior colliculus as reported for other brain structures. The results indicate that ACh plays a neuromodulatory transmitter role in the auditory midbrain by setting the level of neuronal activity. Its exact function in particular behavioral contexts remains to be determined, since the origin of cholinergic innervation of the mammalian IC is still unclear.

The cochlea of Tadarida brasiliensis: specialized functional organization in a generalized bat

Tadarida brasiliensis mexicana employs a broad-band sonar system at frequencies between 80 and 20 kHz and is characterized by non-specialized hearing capabilities. The cochlear frequency map was determined with extracellular horseradish peroxidase tracing in relation to quantitative morphological data obtained with light, scanning and transmission electron microscopy. These data reveal distinct species characteristic specializations clearly separate from the patterns observed in other bats with either broad-band or narrow-band sonar systems. The basilar membrane (BM) is coiled to 2.5 turns and about 12 mm long. Its thickness and width only change within the extreme basal and apical ends. The frequency range from about 30 to 80 kHz is represented in the lower basal turn with a typically mammalian mapping coefficient of about 3 mm/octave. This region exhibits morphological features correlated with non-specialized processing of high frequencies. (1) The BM is radially segmented by thickenings of pars tecta and pars pectinata. (2) The 3 rows of outer hair cells (OHCs) have similar morphology. Between 35 and 86% distance from base, frequencies between 30 and 12 kHz are represented with a slightly expanded mapping coefficient of about 6 mm/octave. In analogy to previous work, this cochlea region is termed acoustic fovea. It includes the frequency range of maximum sensitivity and sharpest tuning (21-27 kHz) but also frequencies below the sonar signals. The fovea is characterized by several morphological specializations. (1) The BM features a continuous radial thickening mainly composed of hyaline substance. (2) There is an increased number of layers of tension fibroblasts in the spiral ligament. (3) There are morphological differences in the arrangements of stereocilia bundles among the 3 rows of OHCs. The transitions between non-specialized and specialized cochlear regions occur gradually within a distance of about 600 microns. The gradients in stereocilia length of both receptor cell types and the gradations in length of the OHC bodies match specialized aspects of the frequency map.

Blurry topography for precise target-distance computations in the auditory cortex of echolocating bats

Echolocating bats use the time from biosonar pulse emission to the arrival of echo (defined as echo delay) to calculate the space depth of targets. In the dorsal auditory cortex of several species, neurons that encode increasing echo delays are organized rostrocaudally in a topographic arrangement defined as chronotopy. Precise chronotopy could be important for precise target-distance computations. Here we show that in the cortex of three echolocating bat species (Pteronotus quadridens, Pteronotus parnellii and Carollia perspicillata), chronotopy is not precise but blurry. In all three species, neurons throughout the chronotopic map are driven by short echo delays that indicate the presence of close targets and the robustness of map organization depends on the parameter of the receptive field used to characterize neuronal tuning. The timing of cortical responses (latency and duration) provides a binding code that could be important for assembling acoustic scenes using echo delay information from objects with different space depths.