John H. Casseday

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 Inferior Colliculus: A Hub for the Central Auditory System

The inferior colliculus (IC) (Fig. 7.1) occupies a strategic position in the central auditory system. Evidence reviewed in this chapter indicates that it is an interface between lower brainstem auditory pathways, the auditory cortex, and motor systems (For abbreviations see Table 7.1). The IC receives ascending input, via separate pathways, from a number of auditory nuclei in the lower brainstem. Moreover, it receives crossed input from the opposite IC and descending input from auditory cortex. These connections suggest that (1) the IC integrates information from various auditory sources and (2) at least some of the integration utilizes cortical feedback. The IC also receives input from ascending somatosensory pathways, suggesting that auditory information is integrated with somatosensory information at the midbrain. Motor-related input to the IC arises from the substantia nigra and globus pallidus. These connections raise the possibility that sensory processing in the IC is modulated by motor action. The major output of the IC is to the auditory thalamocortical system. However, it also transmits information to motor systems such as the deep superior colliculus, and the cerebellum, via the pontine gray. These connections suggest that processing in the IC not only prepares information for transmission to higher auditory centers but also modulates motor action in a direct fashion. In short, the IC is ideally suited to process auditory information based on behavioral context and to direct information for guiding action in response to this information (Aitkin 1986; Casseday and Covey 1996).

Distribution of GABAA, GABAB, and glycine receptors in the central auditory system of the big brown bat, Eptesicus fuscus

Quantitative autoradiographic techniques were used to compare the distribution of GABAA, GABAB, and glycine receptors in the subcortical auditory pathway of the big brown bat, Eptesicus fuscus. For GABAA receptors, the ligand used was 35S‐t‐butylbicyclophosphorothionate (TBPS); for GABAB receptors, 3H‐GABA was used as a ligand in the presence of isoguvacine to block binding to GABAA sites; for glycine, the ligand used was 3H‐strychnine. In the subcortical auditory nuclei there appears to be at least a partial complementarity in the distribution of GABAA receptors labeled with 35S‐TBPS and glycine receptors labeled with 3H‐strychnine. GABAA receptors were concentrated mainly in the inferior colliculus (IC) and medial geniculate nucleus, whereas glycine receptors were concentrated mainly in nuclei below the level of the IC. Within the IC, there was a graded spatial distribution of 35S‐TBPS binding; the most dense labeling was in the dorsomedial region, but very sparse labeling was observed in the ventrolateral region. There was also a graded spatial distribution of 3H‐strychnine binding. The most dense labeling was in the ventral and lateral regions and the weakest labeling was in the dorsomedial region. Thus, in the IC, the distribution of 35S‐TBPS was complementary to that of 3H‐strychnine. GABAB receptors were distributed at a low level throughout the subcortical auditory nuclei, but were most prominent in the dorsomedial part of the IC.

The Lower Brainstem Auditory Pathways

In the auditory system, more than any other sensory modality, extensive processing of incoming signals occurs in the brainstem. In all vertebrates, the auditory pathways below the inferior colliculus consist of a complex system of parallel pathways, each with its own centers for signal processing. The auditory structures of the lower brainstem act as filters to selectively enhance specific stimulus features and as computational centers to add, subtract, or compare signals in different channels. Some brainstem structures, such as the superior olive, have been studied extensively, and their function is at least partially understood. Others, such as the nuclei of the lateral lemniscus, have been largely ignored, and their functional roles are just beginning to be discovered.

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.

The Evolution of Central Pathways and Their Neural Processing Patterns

A comprehensive and conclusive description of the evolution of the central auditory system in vertebrates is a difficult, if not impossible, task. We simply lack important basic information. For instance, we do not know how and what the common ancestors of all the terrestrial vertebrates could hear (certainly not airborne sound, because they had no tympanic middle ear) and how they might have processed basic sounds (such as substrate vibrations). However, a comparative approach allows us to define some principles of auditory processing that we find in all hearing vertebrates and a basic outline of its neural substrate. There is a striking similarity among all vertebrates concerning the principal design of the central auditory system. It. seems to result from the fact that all vertebrate central auditory systems are based on similar basic neural building blocks that work with similar underlying principles. These building blocks were then shaped by evolutionary constraints that were similar for all hearing vertebrates, simply because the acoustic cues that can be used for sound recognition or sound localizations are limited. However, an important issue in this chapter is the increasing evidence that the elaborated central auditory systems in the different clades of recent vertebrates are to a large extent a result of parallel, independent evolution.

Mechanisms for Analysis of Auditory Temporal Patterns in the Brainstem of Echolocating Bats

A vital function of the auditory system in all vertebrates is to identify sounds that are important for social interactions, predation and predator avoidance. Examples of these behaviorally important sounds are communication signals of conspecifics, noises made by movements of other animals and highly specialized species-specific sounds such as the biosonar signals used by echolocating bats. Identification of many behaviorally important sounds, especially those made by prey or predators, must occur rapidly to activate other neural systems that produce a motor response. Many biologically important sounds are characterized by simple temporal features, such as duration of the sound or its components, direction of a frequency sweep, or the rate of modulation in sounds that periodically change in frequency or amplitude. Many sounds are further characterized by complex sequences of elements that follow a specific order over time.

Auditory Pontine Grey: Connections and Response Properties in the Horseshoe Bat

This study investigates the role of the pontine grey as a link between the auditory system and the cerebellum in the bat, Rhinolophus rouxi. We recorded response properties of single neurons in the pontine grey and, in the same preparation, injected wheat germ agglutinin ‐ horseradish peroxidase (WGA‐HRP) in areas responsive to sound. Thus the functional evidence was correlated with retrograde and anterograde transport. The main results are: (i) all auditory neurons in the pontine grey are tuned within one of two harmonically related frequency ranges of the echolocation call. The upper range corresponds to the constant frequency and frequency modulated components of the second harmonic, but the lower range corresponds only to the frequency modulated component of the first harmonic. There is no systematic tonotopic organization; (ii) discharge patterns are extremely variable, latencies cover a wide range, and about half of the neurons are binaurally responsive with excitation from both ears; (iii) most pontine auditory neurons respond preferentially to frequency modulated stimuli; (iv) there is massive input to the pontine grey from the central nucleus of the inferior colliculus; (v) cortical input to the pontine grey does not originate in tonotopically organized auditory cortex. The input is from a dorsal belt area that is specialized for processing combinations of sounds with specific frequency ratios and delays; (vi) projections from the auditory region of the pontine grey are widespread within the cerebellar cortex. The data suggest that the pontine grey transmits to the cerebellum information contained in specific components of the bats biosonar signal.

Spatial tuning of neurons in the inferior colliculus of the big brown bat: effects of sound level, stimulus type and multiple sound sources

We examined factors that affect spatial receptive fields of single units in the central nucleus of the inferior colliculus of Eptesicus fuscus. Pure tones, frequency- or amplitude-modulated sounds, or noise bursts were presented in the free-field, and responses were recorded extracellularly. For 58 neurons that were tested over a 30 dB range of sound levels, 7 (12%) exhibited a change of less than 10° in the center point and medial border of their receptive field. For 28 neurons that were tested with more than one stimulus type, 5 (18%) exhibited a change of less than 10° in the center point and medial border of their receptive field.The azimuthal response ranges of 19 neurons were measured in the presence of a continuous broadband noise presented from a second loudspeaker set at different fixed azimuthal positions. For 3 neurons driven by a contralateral stimulus only, the effect of the noise was simple masking. For 11 neurons driven by sound at either side, 8 were unaffected by the noise and 1 showed a simple masking effect. For the remaining 2, as well as for 5 neurons that were excited by contralateral sound and inhibited by ipsilateral sound, the peak of the azimuthal response range shifted toward the direction of the noise.

Central Auditory Pathways in Directional Hearing

The central auditory system consists of several pathways that parallel one another at some levels of the nervous system and converge or diverge at other levels. The purpose of this chapter is to examine the structure of these pathways for clues to their function in directional hearing. Figure 5-1 introduces the main components, up to the inferior colliculus, of pathways that may be involved in processing cues for directional hearing. The analysis of these pathways will begin at the cochlear nucleus, where all fibers of the auditory nerve terminate (cf Jones and Casseday, 1979). The anteroventral division of the cochlear nucleus is particularly important because it is the origin of pathways to the medial and lateral superior olives, structures that have connections ideally arranged to function as centers for binaural hearing. Other pathways originate in the cochlear nucleus but bypass the superior olivary complex and cross the brain stem to terminate in the nuclei of the lateral lemniscus and inferior colliculus (Fig. 5-1A). These are also considered in this analysis, even though they probably have little to do with binaural interaction at this first level of processing. It will be proposed that the ascending auditory pathways may be divided into binaural and monaural channels. The binaural channels are those pathways in which information from both ears is integrated at the superior olives. Each monaural channel transmits information from the contralateral ear without integration at the superior olives. Evidence reviewed in a later section suggests that this separation of binaural and monaural channels persists to the level of the auditory cortex.