George D. Pollak

Disproportionate frequency representation in the inferior colliculus of doppler-compensating Greater Horseshoe bats: Evidence for an acoustic fovea

Summary1.The inferior colliculus of 8 Greater Horseshoe bats (Rhinolophus ferrumequinun) was systematically sampled with electrode penetrations covering the entire volume of the nucleus. The best frequencies and intensity thresholds for pure tones (Fig. 2) were determined for 591 neurons. The locations of the electrode penetrations within the inferior colliculus were histologically verified.2.About 50% of all neurons encountered had best frequencies (BF) in the frequency range between 78 and 88 kHz (Table 1, Fig. 1A). Within this frequency range the BFs between 83.0 and 84.5 kHz were overrepresented with 16.3% of the total population of neurons (Fig. 1B). The frequencies of the constant frequency components of the echoes fall into this frequency range.3.The representation of BFs expressed as number of neurons per octave shows a striking correspondence to the nonuniform innervation density in the afferent innervation of the basilar membrane (Bruns and Schmieszek, in press). The high innervation density of the basilar membrane in the frequency band between 83 and 84.5 kHz coincides with the maximum of the distribution of number of neurons per octave across frequency in the inferior colliculus (Fig. 1 C).4.The disproportionate representation of frequencies in the auditory system of the greater horseshoe bat is described as an acoustical fovea functioning in analogy to the fovea in the visual system. The functional importance of the Doppler-shift compensation for such a foveal mechanism in the auditory system of horseshoe bats is related to that of tracking eye movements in the visual system.

The Neural Basis of Echolocation in Bats

The brain of an echo locating bat is devoted, in large part, to analyzing sound and conducting behavior in a world of sounds and echoes. This monograph is about analysis of sound in the brainstem of echolocating bats and concerns the relationship between brain structure and brain function. Echolocating bats are unique subjects for the study of such relationships. Like man, echolocating bats emit sounds just for the purpose of listening to them. Simply by observing the bats echolocation sounds, we know what the bat listens to in nature. We therefore have a good idea what the bats auditory brain is designed to do. But this alone does not make the bat unique. The brain of the bat is, by mammalian standards, rather primitive. The unique aspect is the combination of primitive characteristics and complex auditory processing. Within this small brain the auditory structures are hypertrophied and have an elegance of organization not seen in other mammals. It is as if the auditory pathways had evolved while the rest of the brain remained evolutionary quiescent.

The effects of GABAergic inhibition on monaural response properties of neurons in the mustache bat's inferior colliculus

The effects of GABAergic inhibition on response properties of neurons in the inferior colliculus were investigated. The experimental animals were mustache bats and responses were monitored from neurons in the hypertrophied 60 kHz isofrequency contour of the inferior colliculus. The features we report on here are: 1) the maximum discharge rates evoked by tone bursts at each units best frequency; 2) the forms of the rate-level functions; 3) the discharge patterns evoked by best frequency tone bursts; and 4) the changes in these response features that were observed when GABAergic inhibition was blocked with bicuculline, an antagonist specific for GABAA receptors. There were three main findings. The first is that bicuculline caused the discharge rate to increase in the majority of neurons. The maximum firing rates in more than half of the units increased by at least 100%, and in 15% of the cells the maximum spike-count increased 400% or more. Of particular interest were the 13 cells that were nearly unresponsive to any tone burst, but responded vigorously to the same stimuli after application of bicuculline. The second main finding is that the increased discharge rates were due either to a change from a phasic to a tonic discharge pattern, or to a change in overall excitability with no change in discharge pattern. The third main finding was that bicuculline changed the shape of the rate-level functions in almost half of the cells studied. The general trend was that units whose pre-drug rate-level functions were upper-threshold were most likely to be changed, followed by regular nonmonotonic and non-saturated monotonic. Units with saturated monotonic functions were the least likely to be affected by bicuculline. These results lead us to suggest that GABAergic inhibition acts on collicular cells in two principal ways. The first way is to modify the effects of the excitatory innervation and thereby shape the response features of collicular neurons. The formation of rate-level functions is but one illustration of the shaping action of GABAergic inhibition. Other features that are shaped by GABAergic inhibition include discharge patterns, thresholds, latencies and tuning curves. The second way is to provide a regulated suppression of evoked activity. We propose that the suppression is situation dependent and may act to enhance the operating range of collicular neurons in situations of particular importance to the animal, such as during periods of selective attention and perhaps in other situations as well.

Dissecting the circuitry of the auditory system

Abstract The brainstem auditory system is a complex system composed of numerous parallel and serial pathways that converge on a common destination in the inferior colliculus (IC). The exact nature of the response transformations that occur in the IC have, however, been elusive – even though the IC has been the subject of numerous studies for more than 30 years. Recent studies have addressed this issue by recording from IC neurons before and during micro-iontophoresis of drugs that selectively block GABA A or glycine receptors (the dominant inhibitory receptors in the IC) or by reversibly inactivating a lower nucleus that provides inhibitory innervation to the IC. These studies have revealed some of the ways that signals, relayed via many different parallel routes, interact in the IC, and suggest some functional advantages that these interactions might have.

Syllable acoustics, temporal patterns, and call composition vary with behavioral context in Mexican free-tailed bats

Recent research has shown that some bat species have rich vocal repertoires with diverse syllable acoustics. Few studies, however, have compared vocalizations across different behavioral contexts or examined the temporal emission patterns of vocalizations. In this paper, a comprehensive examination of the vocal repertoire of Mexican free-tailed bats, T. brasiliensis, is presented. Syllable acoustics and temporal emission patterns for 16 types of vocalizations including courtship song revealed three main findings. First, although in some cases syllables are unique to specific calls, other syllables are shared among different calls. Second, entire calls associated with one behavior can be embedded into more complex vocalizations used in entirely different behavioral contexts. Third, when different calls are composed of similar syllables, distinctive temporal emission patterns may facilitate call recognition. These results indicate that syllable acoustics alone do not likely provide enough information for call recognition; rather, the acoustic context and temporal emission patterns of vocalizations may affect meaning.

Spectrotemporal Receptive Fields in the Inferior Colliculus Revealing Selectivity for Spectral Motion in Conspecific Vocalizations

Frequency modulations are a prominent feature of animal vocalizations and human speech. Here we investigated how neurons in the inferior colliculus (IC) of Mexican free-tailed bats respond to the frequency-modulated (FM) direction and velocity of complex signals by extracting their spectrotemporal receptive fields (STRFs) using a family of upward- and downward-moving ripple stimuli. STRFs were obtained in more than half of the cells that were sampled. To verify the validity of each STRF, we compared their features both with tone-evoked responses and by convolving the STRF with several conspecific calls. We show that responses to tones are in close agreement with the STRF and that the responses predicted by convolutions compare favorably with responses evoked by those calls. The high predictability showed that the STRF captured most of the excitatory and inhibitory properties of IC cells. Most neurons were selective for the direction and velocity of spectral motion with a majority favoring the downward FM direction, and most had spectrum–time inseparability that correlated with their direction selectivity. Furthermore, blocking inhibition significantly reduced the directional selectivity of these neurons, suggesting that inhibition shapes FM direction selectivity in the IC. Finally, we decomposed the natural calls into their ripple components and show that most species-specific calls have downward-sweeping FM components with sweep velocities that correspond with the preferred sweep velocities of IC neurons. This close quantitative correspondence among features of signals and responses suggests that IC cells are tuned by inhibition to respond optimally to spectral motion cues present in their conspecific vocalizations.

Time is traded for intensity in the bat's auditory system.

Disparities in time and intensity are the two chief cues animals use for localizing a sound source in space. Echolocating bats belonging to the family Molossidae emit brief, ultrasonic signals for orientation that sweep downward about an octave over the duration of the pulse. Due to acoustic shadowing and the directional properties of the ears, pronounced interaural intensity disparities are created that vary as a function of azimuth. However, due to the small headwidth of these animals, azimuthal changes create small interaural time disparities that are at most 30 microseconds. The experiments in this report are concerned with the binaural processing of time and intensity disparities using brief FM signals that simulate the animals natural echolocation calls. Binaural neurons receiving excitation from one ear and inhibition from the other (E-I neurons) were recorded from the inferior colliculus of Mexican free-tailed bats. The majority of units sampled were highly sensitive for temporal disparities of 100-300 microseconds, and a few had significant changes in discharge probability when interaural time was changed by 10-20 microseconds. However, all E-I neurons were also sensitive to intensity disparities. With only one exception, all E-I neurons traded time for intensity. On the average, each decibel difference in intensity could be compensated for by advancing or delaying the inhibitory sound by 47 microseconds. The main conclusion is that the auditory system processes interaural disparities by transforming level differences at the two ears into latency differences. Thus the discharge probability of each binaural neuron is determined largely by the arrival times of the discharges from the excitatory and inhibitory ears. In view of the substantial time-intensity trading ratios, the small interaural time disparities produced by azimuthal locations off the midline play no role in shaping the response properties of these neurons. Specific examples of how time-intensity trades can translate into a high spatial selectivity are presented.

Roles of inhibition for transforming binaural properties in the brainstem auditory system

This review is concerned with the operation of circuits in the central auditory system, how they transform response features and what functional significance may be attributed to those transformations. We focus on the role that GABAergic inhibition plays in processing interaural intensity disparities (IIDs), the principal cues for localizing high frequencies, and the transformations of IID coding that occur between the superior olivary complex and the inferior colliculus (IC). IIDs are coded by excitatory-inhibitory (EI) cells, so called because they are excited by one ear and inhibited by the other. EI neurons are first created in the lateral superior olive (LSO), but they also dominate the dorsal nucleus of the lateral lemniscus (DNLL) and regions of the IC. The three nuclei are intimately linked through a complex arrangement of excitatory and inhibitory connections. One of these is a crossed excitatory projection from the LSO to both the DNLL and IC. The binaural properties of EI neurons in LSO, DNLL and IC appear strikingly similar, suggesting that the EI properties created in the LSO are simply imposed on the DNLL and IC through the crossed excitatory projections. Recent studies support the idea that EI properties created in lower centers are imposed on some IC cells. However, other studies show that the circuitry linking LSO, DNLL and IC generates a number of response transformations in many IC cells. These transformations include marked changes in EI properties with stimulus duration, the generation of highly focused spatial receptive fields, shifts in sensitivity to IIDs, and the de novo creation of the EI response property. All of these transformations are produced by inhibitory innervation of the IC. An additional emergent property is also imposed on IC cells that receive GABAergic innervation from the DNLL. That property is a change in the binaural features of the IC cell, a change produced by the reception of an earlier sound whose IID is strongly excitatory to the IC cell. We illustrate each of these transformations, propose circuitry that could account for the observed properties and suggest some functional relevance for each. In the final section, we discuss some of the inherent uncertainties associated with attributing functional consequences to response features and then consider whether the transformations found in some mammals are species-specific or are universal features of all mammals.

Binaural processing in the dorsal nucleus of the lateral lemniscus.

We studied the binaural properties of 72 neurons in the dorsal nucleus of the lateral lemniscus (DNLL) of the mustache bat. There are six main findings: 1) Conventional EI neurons that were excited by stimulation of the contralateral ear and inhibited by ipsilateral stimulation, comprise the majority (80%) of binaural DNLL cells. 2) For most EI neurons the quantitative features of their interaural intensity disparity (IID) functions, maximum inhibition, dynamic range and 50% point IIDs, were largely unaffected by the absolute intensity at the contralateral ear. 3) Although the net effect of the inhibition evoked by ipsilateral stimulation was to suppress discharges evoked by contralateral stimulation, our results indicate that the inhibitory inputs can act in three different ways. The first was a time-intensity trade, where increasing the intensity at the ipsilateral ear evoked inhibitory effects with progressively shorter latencies. The second way was that the latency of inhibition did not appear to decrease with ipsilateral intensity, but rather increasing ipsilateral intensity appeared only to increase the strength of the inhibition. The third way was that the lowest effective ipsilateral intensity suppressed the first spikes evoked by the contralateral stimulus and higher ipsilateral intensities then suppressed the later discharges of the train. Each of these inhibitory patterns was seen in about a third of the cells. 4) Neurons that had more complex binaural properties, such as the facilitated EI neurons (EI/F) and neurons that were driven by sound to either ear (EE neurons), represented about 20% of the binaural population. There were two types of EE neurons; those in which there was a simple summation of discharges evoked with certain IIDs, and those in which the spike-counts to binaural stimulation at certain IIDs were greater than a summation of the monaural counts and thus were facilitated. 5) All binaural neurons were strongly inhibited with IIDs that favored the ipsilateral ear. Our findings indicate that the more complex binaural types, the facilitated EI neurons (EI/F) as well as the two types of EE neurons, may be constructed from conventional EI neurons by adding inputs from several sources that impart the more complex features to these neurons. We propose four circuits that could account for the different binaural response properties that we observed. The circuits are based on the known connections of the DNLL and the neurochemistry of those connections. Finally, we compared the binaural properties of neurons in the mustache bat DNLL with those of neurons in the mustache bat inferior colliculus and lateral superior olive.(ABSTRACT TRUNCATED AT 400 WORDS)

Rethinking Tuning: In Vivo Whole-Cell Recordings of the Inferior Colliculus in Awake Bats

Tuning curves were recorded with patch electrodes from the inferior colliculus (IC) of awake bats to evaluate the tuning of the inputs to IC neurons, reflected in their synaptic tuning, compared with the tuning of their outputs, expressed in their discharge tuning. A number of unexpected features were revealed with whole-cell recordings. Among these was that most neurons responded to tones with inhibition and/or subthreshold excitation over a surprisingly broad frequency range. The synaptic tuning in many cells was at least 1.5–2.0 octaves wide and, on average, was more than twice as wide as the frequency range that evoked discharges even after inhibition was blocked. In most cells, tones evoked complex synaptic response configurations that varied with frequency, suggesting that these cells were not innervated by congruent excitatory and inhibitory projections. Synaptic tuning was not only wide but was also diverse, in which some cells were dominated by excitation (n = 20), others were dominated by excitation with sideband inhibition (n = 21), but most were dominated by inhibition with little evidence of excitation (n = 31). Another unexpected finding was that some cells responded with inhibition to the onset and offset of tones over a wide frequency range, in which the patterns of synaptic responses changed markedly with frequency. These cells never fired to tones at 50 dB sound pressure level but fired to frequency-modulated sweeps at that intensity and were directionally selective. Thus, the features revealed by whole-cell recordings show that the processing in many IC cells results from inputs spectrally broader and more complex than previously believed.