Handbook of Mammalian Vocalization

An Integrative Neuroscience Approach

Stefan M Brudzynski

• Publisher: Academic Press
• Year: 2009
• ISBN:
  9780080923376
• Topic: Psychology
• Subtopic: Neuropsychology
• Index: Psychology

Handbook of Mammalian Vocalization is designed as a broad and comprehensive, but well-balanced book, written from the neuroscience point of view in the broad sense of this term. This well-illustrated Handbook pays particular attention to systematically organized details but also to the explanatory style of the text and internal cohesiveness of the content, so the successive chapters gradually develop a consistent story without losing the inherent complexity. Studies from many species are included, however rodents dominate, as most of the brain investigations were done on these species.

The leading idea of the Handbook is that vocalizations evolved as highly adaptive specific signals, which are selectively picked up by the brain. The brain serves as a receptor and behavioural amplifier. Brain systems will be described, which allow vocal signals rapidly changing the entire state of the organism and trigger vital biological responses, usually also with accompanying emission of vocalizations. Integrative brain functions leading to vocal outcome will be described, along with the vocalization generators and motor output to larynx and other supportive motor subsystems. The last sections of the Handbook explains bioacoustic structure of vocalizations, present understanding of information coding, and origins of the complex semiotic/ semantic content of vocalizations in social mammals.

The Handbook is a major source of information for professionals from many fields, with a neuroscience approach as a common denominator. The handbook provides consistent and unified understanding of all major aspects of vocalization in a monographic manner, and at the same time, gives an encyclopaedic overview of major topics associated with vocalization from molecular/ cellular level to behavior and cognitive processing. It is written in a strictly scientific way but clear enough to serve not only for specialized researchers in different fields of neuroscience but also for academic teachers of neuroscience, including behavioural neuroscience, affective neuroscience, clinical neuroscience, neuroethology, biopsychology, neurolingusitics, speech pathology, and other related fields, and also for research fellows, graduate and other advanced students, who widely need such a source publication.

• The first comprehensive handbook on what we know about vocalization in Mammalians
• Carefully edited, the handbook provides an integrated overview of the area
• International list of highly regarded contributors, including Jaak Pankseep (Washington State University), David McFarland (Oxford), John D. Newman (NIH? Unit on Developmental Neuroethology), Gerd Poeggel (Leipzig), Shiba Keisuke (Chiba City, Japan), and others, tightly edited by a single, well regarded editor who has edited a special issue in Behavioral Brain Research on the topic before

SECTION 1

Introduction

CHAPTER 1.1

Vocalization as an ethotransmitter: introduction to the Handbook of Mammalian Vocalization

Stefan M. Brudzynski

Department of Psychology, Brock University, St. Catharines, Ontario, Canada

I. Introduction

Animal vocal communication has received much attention from researchers for many decades. Over the last 70 years, attention has been focused on different aspects of the process of sending and receiving signals. Some approaches were centered on the mechanisms of emitting vocalizations, regardless of the recipient, and others represented a unidirectional process of producing and sending vocal signals by the signaler to the receiver. Adequate responses by the receiver were evidence of the communicatory process. Also, significant research attention has been focused on receivers with regard to the behavioral consequences of perceived species-specific vocal signals. Finally, vocal communication was also approached as an exchange of vocalizations between or among animals in a process of bi- or multidirectional communication, where the main biological function was centered not on sending or receiving specific information, but on testing the responsiveness of the receiver or influencing the receiver’s behavior. In larger social groups, this type of communication could be seen as a social negotiation or social decision-making process.

The fundamental and common element of all of these different approaches is vocalization as a biological phenomenon, and this is the main subject of this handbook.

I.A. Mammalian vocalization as a particularly well-developed communication system

Despite numerous modes of mammalian communication, the production of vocalizations in mammals remains one of the most widespread behavioral and physiological processes, requiring highly complex coordination and integration of numerous subsystems, including the central nervous system, autonomic and endocrine systems, and peripheral organs. There are several biological reasons why vocalization is found ubiquitously among mammalian species regardless of their habitat (subterrean, terrestrial, aerial, or aquatic). Acoustic signals can propagate for considerable distances, and their reception is dependent neither on daylight, nor on good visibility. Vocalizations may be produced and terminated almost instantly (with negligible latency), and the discontinued signals do not leave any permanent trace. Finally, the combination of different acoustic parameters within calls provides an immensely rich combination of features for encoding signals. As a consequence, all mammalian vocalizations represent a theoretically unlimited repertoire of biological signals, which may differ from each other just as individual mammalian organisms differ within any species. Finally, vocal signals have also been used for rapid echolocation (as self-communication) in aerial and some aquatic mammals. There is no other communication method (visual, olfactory, thermal, or electromagnetic) which can combine all these features together and which has been subjected to such a phylogenetic variation. One of the goals of this handbook is to recognize this uniqueness of vocalizations as mammalian communication signals.

During intraspecific interactions, all mammals use combinations of communication modes (e.g., vocal, visual and olfactory, or visual, vocal and tactile), and all these signals have the capability of affecting the behavior of recipients. Communication based on direct contact, both mechanical and/or chemical, is phylogenetically older, while communication based on telereception appeared later in evolution. Among telereception modes, electroreception and distant chemoreception (pheromones) seem to have appeared earlier in evolution than visual and vocal communication, which can convey reliable signals for the longest distances. Among these last two communication methods, vocalization has reached the highest sophistication in mammals as a group. Vocal signals have reached considerable levels of complexity, and can usually travel for longer distances than those determined by visual range. Thus, all mammalian communicatory signals may be classified according to their evolutionary history, with a gradually increasing range of operation and signal complexity. This observation leads to the conclusion that vocalization is the most recent and advanced mode of communication. Vocalization also has its own evolutionary history within the mammalian taxon, from simple vocal displays, through complex vocalization signaling to semiotically- and referentially-organized vocal communication. Examples of all these stages of mammalian vocal communication are represented in this handbook. The evolutionary development of vocal communication may be documented not only for mammals, but also for birds, which are known to produce sophisticated vocalizations.

I.B. The neuroscience approach in studies of mammalian vocalization

Direct studies of brain mechanisms involved in producing vocalizations, and of the central mechanisms of reception, recognition and analysis of species-specific calls, provide additional approaches to the topic and reveal many aspects of mammalian vocal communication. Since Charles Darwin published The Expression of the Emotions in Man and Animals in 1872 (Darwin, 1872/1889), behavioral sciences, including comparative psychology, have struggled for almost 140 years to explain clearly the biological nature and origin of vocal communication in mammals. One of the obstacles was, and still is, our inability to know the subjective feelings and intentions of animals when they emit vocalizations. One of the ways to gain some insight into this issue is to use a comparative and multidisciplinary approach, as is richly illustrated in this handbook. This includes using a comparative approach to identify functions of the brain structures and systems which are directly involved in the production of vocalizations. The high degree of homology in transmitters, brain structures and neural regulation underlying the production of vocalizations among different groups of animals, and among animals and humans, represents the most powerful evidence of a common origin of internal states, particularly affective states, and common biological reasons for communicating. The subtitle of this handbook, An Integrative Neuroscience Approach, illustrates well one of the main goals of the book: to gain a better understanding of why the vocal communication system evolved in mammals, how vocal production is controlled by the brain, what neural factors influence production and reception of vocalizations, and what physiological, behavioral, affective and cognitive processes are involved in this process.

II. The concept of ethotransmitter

All modes of communication may be regarded as behavioral initiators, modulators, or inhibitors, depending on the situation, state of the organism and structure of the signal. Although all communicating signals, regardless of their mode, may fulfill the criteria of behavioral transmitters, vocalization may serve as a particularly good example. A behavioral transmitter may be defined as a relatively weak physical or chemical stimulus originating from one organism, which is capable of inducing energetically costly responses in another organism through elevated activity of the central nervous system and activation of the somatic, autonomic and endocrine systems.

The function of behavioral transmitters is analogous to the action of neurotransmitters in the brain. While the latter operates among individual cells, the former operates among individual organisms. Binding of a neurotransmitter molecule to its receptor can activate the entire neuron, central nervous system, or the entire organism, where the energy of the resulting process (from utilization of ATP) initiates a response with much higher output energy than the initial energy of the stimulus molecule. Both situations, at the molecular and organism levels, have an initial biological stimulus (a signaling molecule or vocal signal), which can affect specialized receptors (pharmacological or physiological), involve action of the central nervous system, and cause an amplified response of neuronal systems or an entire organism, respectively. The action of these transmitters is based on the “lock-and-key” principle, where the transmitter is the key and the lock is the receptor capable of initiating an amplified response.

Using the analogy to neurotransmitters, behavioral transmitters could be termed ethotransmitters (from the Greek ethos meaning “character,” “habit,” “behavior” plus the Latin transmissio, meaning “sending across”). Which communicatory signals should be termed ethotransmitters, and at what evolutionary level they should act, are undoubtedly debatable points. Nevertheless, mammalian vocalization represents the best developed example of the postulated ethotransmitter, and it deserves special attention. This term not only signifies a characteristic biological phenomenon, but also provides a new framework for the understanding of the evolution of vocalization and vocal communication, and their biological roles in social animals. Moreover, a better understanding of mammalian vocalization as ethotransmitter may provide us with a basis for a full understanding of the origin of human speech. A provisional definition of ethotransmitter is suggested below.

The “lock-and-key” metaphor has been mentioned frequently for neurotransmitter action for more than a century, and was also noted a long time ago for behavioral transmission. This metaphor was used by Konrad Lorenz in his studies of bird behavior. The signaling stimuli were termed releasers, which were capable of releasing specific behavior in the receivers by acting on the central nervous system and activating the innate releasing mechanism (Lorenz, 1935). The concept of the “innate releasing mechanism” (Tinbergen, 1951) or “inborn releasing scheme” (Uexküll von, 1934) emphasized the specific relationship between the character of a particular stimulus and a particular stereotypic response released. The ethological studies which followed, however, were trapped within the narrow framework of these concepts by trying to generalize the behavior of all animals from invertebrates to vertebrates within this conceptual scheme, and by assuming that the released responses are instinctive, i.e., innate and largely mechanistic in nature. This introduction does not allow for a detailed description of the history of these concepts in the abundant ethological literature over the last 70 years. However, it might not be an essential topic for this handbook, because the best known classical ethological textbooks summarizing substantial ethological knowledge paid little attention to neural mechanisms of behavior, and marginal attention to mammalian vocalization (Hinde, 1966; Eibl-Eibesfeldt, 1970; Immelmann, 1980). As mentioned previously, studies of the role of the central nervous system in the process of communication are essential for understanding this phenomenon, and to shape our understanding of vocalization as an ethotransmitter.

An ethotransmitter produced during mammalian social behavior should fulfill the following criteria:

1. It should have evolved to play an adaptive role in regulating behavior, particularly in highly social animals;

2. It should be produced and released by specialized tissues and organs;

3. Production and emission of the transmitter should be controlled by the central nervous system;

4. It should be predominantly targeted at other organisms of the same species, and emission of the ethotransmitter should occur in a way that maximizes its reception and behavioral effects on the recipients;

5. It should have characteristic structure suitable for transmission from one organism to another;

6. It should be selectively recognized by receptive mechanisms of the recipient organisms;

7. It should have properties of activating the central nervous system of the recipient and amplifying its responses (both in the sense of behavioral excitation or inhibition);

8. It should have the capability of inducing differential responses in the recipients, depending on the transmitter structure and mode of release.

Mammalian vocalization fulfills all of these criteria. The Handbook of Mammalian Vocalization is organized in such a way that successive sections of the book discuss evidence for one or more of the points listed above. The main sections of the handbook deal with the evolution and variability of vocalizations, production and emission, transmission and reception of calls, as well as responses of the recipients, mechanisms of generation of amplified responses, generation of sound and semiotic content of emitted vocalizations.

III. Overview of the content of this handbook

The content of the handbook is organized in ten sections, with 4–6 individual chapters in each section. The order of sections roughly follows the criteria listed for an ethotransmitter, except for Section 1, which forms an introduction.

III.A. Section 2

Section 2 provides exemplary studies of evolution of the vocal system and vocalization. The larynx is the chief organ for the production of vocalizations in mammals, and the evolution of its specialized muscles is described by Joseph Hoh. Some other aspects of larynx evolution are also mentioned in Section 10, dealing with the mechanism of sound production. Parallel to the evolution of the components needed for the physical production of vocalizations, a complex neural control needed to evolve. An overview of the core neural system in the mammalian brain responsible for such control is outlined by John Newman. The evolution of particular mammalian groups may differ significantly, depending on the environment in which the organisms live, their biological adaptations and social organization. Rodents represent an interesting group which has developed a fast reproduction cycle with infants being born at a relatively undeveloped (altricial) stage. It is interesting that these altricial infants can communicate by ultrasonic vocalization with their mother. Myron Hofer discusses the evolution of infant rat separation calls and their adaptive role. Other details of infant rat vocalizations and their adaptations are provided in Section 6. As another example, Alanna Maltby and co-workers from Gareth Jones’ laboratory explain the evolutionary origin of bat echolocation calls. Other aspects of evolution and specific functions of the larynx are provided in Section 10.

III.B. Section 3

Mammalian vocalizations have evolved in many directions. Examples of this diversity are provided in Section 3. One general rule is that the sound frequency range of basic vocalizations produced by vibration of the vocal folds remains in proportion to the body mass of the vocalizing organism. The larger the body mass, the lower the sound frequency. This relationship is described by Neville Fletcher. In general, mammalian vocalizations may range from infrasounds to ultrasounds (i.e., below and above human hearing range). While infrasounds evolved for long-distance communication, ultrasonic calls serve for short-range communication. This is discussed in chapters written by Michael Garstang about elephant vocalizations and by Neville Fletcher with my coauthorship about rat vocalizations. These chapters explain how vocalizations are structured and emitted in order to maximize their reception by other members of the species. The largest number of mammalian species is represented by rodents. Almost all of them have developed an effective system of ultrasonic communication with a considerable acoustic repertoire. Examples of a very high variability of these calls are described in two chapters, by Gillian Sales for adult wild and wildtype rodent species, and by Maria Luisa Scattoni and Igor Branchi for mouse infants of different laboratory strains.

III.C. Section 4

One of the criteria listed for an ethotransmitter is its selective recognition by recipients. Section 4 summarizes evidence that the mammalian brain has mechanisms responsible for the selective recognition of species-specific vocalizations. The selective perception and recognition of vocal signals are summarized by Günter Ehret and Simone Kurt. Selective responses to vocal signals may be found at different levels of the central nervous system, from subcortical regions to the neocortex. Markus Wöhr and Rainer Schwarting, working on rats, report that although the semiotic content of calls may require learning, there is an innate preparedness to do so. Josef Syka describes activation of other subcortical structures in guinea pigs, and concludes that the detection of species-specific vocalizations is not based on “call detectors” but on encoding the spectrotemporal acoustic patterns of vocalization by specialized circuits. Finally, Christopher Petkov and his colleagues, from the laboratory of Nikos Logothetis, describe a specific cortical region in the primate brain which is activated by species-specific vocalizations and is homologous to the human voice recognition region.

III.D. Section 5

Section 5 presents evidence that species-specific vocalizations activate the central nervous system and behavior. Yoav Litvin, from the laboratories of Caroline Blanchard and Robert Blanchard, describes the initiation of specific defensive responses of rats to alarm vocalizations. Markus Wöhr and colleagues, working in the laboratory of Francesca D’Amato, discuss the effects of altricial rodent pup vocalizations on the behavior of their mother. A subsequent chapter provides further evidence that species-specific vocalizations are effective triggers of affective behavior in recipients, as reported by Koji Kuraoka and Katsuki Nakamura in the monkey. Finally, vocalizations may...

Table of contents

• Cover
• Title
• Copyright
• Contents
• About the Authors
• Preface
• Acknowledgments
• Section 1. Introduction
• Section 2. Evolution of the Vocal System and Vocalization
• Section 3. Diversity of Vocalizations
• Section 4. Vocalizations as Specific Stimuli: Selective Perception of Vocalization
• Section 5. Effects of Vocalization on the Organism’s State and Behavior: Brain as an Amplifier of Vocal Signals
• Section 6. Limbic Generation of Vocalization: Vocalization as an Index of Behavioral State
• Section 7. Hypothalamic/Limbic Integrative Function for Vocal/Behavioral Outcome
• Section 8. Midbrain and Central Pattern Generators for Vocalization
• Section 9. Integrative Motor Functions of the Ambiguus, Retroambiguus and Parabrachial Nuclei
• Section 10. Sound Production by Larynx
• Section 11. Vocal Communication Systems in Mammals: Semiotic Codes in Vocalization
• Index
• Color Plates