Neuroethology
Encyclopedia
Neuroethology is the evolutionary and comparative approach to the study of animal behavior and its underlying mechanistic control by the nervous system. This interdisciplinary branch of behavioral neuroscience
endeavors to understand how the central nervous system translates biologically relevant stimuli into natural behavior. For example, many bats are capable of echolocation
which is used for prey capture and navigation. The auditory system of bats is often cited as an example for how acoustic properties of sounds can be converted into a sensory map of behaviorally relevant features of sounds. Neuroethologists hope to uncover general principles of the nervous system from the study of animals with exaggerated or specialized behaviors.
As its name implies, neuroethology is a multidisciplinary field composed of neurobiology (the study of the nervous system) and ethology
(the study of behavior in natural conditions). A central theme of the field of neuroethology, delineating it from other branches of neuroscience, is this focus on natural behavior. Natural behaviors may be thought of as those behaviors generated through means of natural selection
(i.e. finding mates, navigation, locomotion, predator avoidance) rather than behaviors in disease states, or behavioral tasks that are particular to the laboratory.
The scope of neuroethological inquiry might be summarized by Jörg-Peter Ewert
, a pioneer of neuroethology, when he considers the types of questions central to neuroethology in his 1980 introductory text to the field:
Often central to addressing questions in neuroethology are comparative methodologies, drawing upon knowledge about related organisms’ nervous systems, anatomies, life histories, behaviors and environmental niches. While it is not unusual for many types of neurobiology experiments to give rise to behavioral questions, many neuroethologists often begin their research programs by observing a species’ behavior in its natural environment. Other approaches to understanding nervous systems include the systems identification approach, popular in engineering
. The idea is to stimulate the system using a non-natural stimulus with certain properties. The system's response to the stimulus may be used to analyze the operation of the system. Such an approach is useful for linear
systems, but the nervous system is notoriously nonlinear, and neuroethologists argue that such an approach is limited. This argument is supported by experiments in the auditory system. These experiments show that neural responses to complex sounds, like social calls, can not be predicted by the knowledge gained from studying the responses due to pure tones (one of the non-natural stimuli favored by auditory neurophysiologists). This is because of the non-linearity of the system.
Modern neuroethology is largely influenced by the research techniques used. Neural approaches are necessarily very diverse, as is evident through the variety of questions asked, measuring techniques used, relationships explored, and model systems employed. Techniques utilized since 1984 include the use of intracellular dyes, which make maps of identified neurons possible, and the use of brain slices, which bring vertebrate brains into better observation through intracellular electrodes (Hoyle 1984). Currently, other fields toward which neuroethology may be headed include computational neuroscience
, molecular genetics
, neuroendocrinology
. The existing field of neural modeling may also expand into neuroethological terrain, due to its practical uses in robotics
. In all this, neuroethologists must use the right level of simplicity to effectively guide research towards accomplishing the goals of neuroethology.
Critics of neuroethology might consider it a branch of neuroscience concerned with ‘animal trivia’. Though neuroethological subjects tend not to be traditional neurobiological model systems (i.e. Drosophila
, C. elegans
, or Danio rerio
), neuroethological approaches emphasizing comparative methods have uncovered many concepts central to neuroscience as a whole, such as lateral inhibition
, coincidence detection, and sensory maps
. The discipline of neuroethology has also discovered and explained the only vertebrate behavior for which the entire neural circuit has been described: the electric fish
jamming avoidance response
. Beyond its conceptual contributions, neuroethology makes indirect contributions to advancing human health. By understanding simpler nervous systems, many clinicians have used concepts uncovered by neuroethology and other branches of neuroscience
to develop treatments for devastating human diseases.
as a unique discipline within the discipline of Zoology
. Although animal behavior had been studied since the time of Aristotle
(384-342 BC), it was not until the early twentieth century that ethology finally became distinguished from natural science (a strictly descriptive field) and ecology. The main catalysts behind this new distinction were the research and writings of Konrad Lorenz
and Niko Tinbergen.
Konrad Lorenz was born in Austria in 1903, and is widely known for his contribution of the theory of fixed action pattern
s (FAPs): endogenous, instinctive behaviors involving a complex sequence of movements that are triggered (“released”) by a certain kind of stimulus. This sequence always proceeds to completion, even if the original stimulus is removed. It is also species-specific and performed by nearly all members. Lorenz constructed his famous “hydraulic model” to help illustrate this concept, as well as the concept of action specific energy, or drives.
Niko Tinbergen was born in the Netherlands in 1907 and worked closely with Lorenz in the development of the FAP theory; their studies focused on the egg retrieval response of nesting geese. Tinbergen performed extensive research on the releasing mechanisms of particular FAPs, and used the bill-pecking behavior of baby herring gulls as his model system. This led to the concept of the supernormal stimulus. Tinbergen is also well known for his four questions
that he believed ethologists should be asking about any given animal behavior; among these is that of the mechanism of the behavior, on a physiological, neural and molecular level, and this question can be thought of in many regards as the keystone question in neuroethology. Tinbergen also emphasized the need for ethologists and neurophysiologists to work together in their studies, a unity that has become a reality in the field of neuroethology.
Unlike behaviorism
, which studied animals' reactions to non-natural stimuli
in artificial, laboratory
conditions, ethology sought to categorize and analyze the natural behaviors of animals in a field setting. Similarly, neuroethology asks questions about the neural bases of naturally occurring behaviors, and seeks to mimic the natural context as much as possible in the laboratory.
Although the development of ethology as a distinct discipline was crucial to the advent of neuroethology, equally important was the development of a more comprehensive understanding of Neuroscience
. Contributors to this new understanding were the Spanish Neuroanatomist, Ramon y Cajal (born in 1852), and physiologists Charles Sherrington, Edgar Adrian, Alan Hodgkin, and Andrew Huxley
. Charles Sherrington, who was born in Great Britain in 1857, is famous for his work on the nerve synapse as the site of transmission of nerve impulses, and for his work on reflexes in the spinal cord. His research also led him to hypothesize that every muscular activation is coupled to an inhibition of the opposing muscle. He was awarded a Nobel Prize for his work in 1932 along with Lord Edgar Adrian who made the first physiological recordings of neural activity from single nerve fibers.
Alan Hodgkin and Andrew Huxley
(born 1914 and 1917, respectively, in Great Britain), are known for their collaborative effort to understand the production of action potentials in giant squid neurons. The pair also proposed the existence of ion channels to facilitate action potential initiation, and were awarded the Nobel Prize in 1963 for their efforts.
As a result of this pioneering research, many scientists then sought to connect the physiological aspects of the nervous and sensory systems to specific behaviors. These scientists – Karl von Frisch
, Erich von Holst
, and Theodore Bullock – are frequently referred to as the “fathers” of neuroethology. Neuroethology did not really come into its own, though, until the 1970s and 1980s, when new, sophisticated experimental methods allowed researchers such as Masakazu Konishi
, Walter Heiligenberg
, Jörg-Peter Ewert
, and others to study the neural circuits underlying verifiable behavior.
Its membership draws from many research programs around the world; many of its members are students and faculty members from medical schools and neurobiology departments from various universities. Modern advances in neurophysiology
techniques have enabled more exacting approaches in an ever-increasing number of animal systems, as size limitations are being dramatically overcome. Survey of the most recent (2007) congress of the ISN meeting symposia topics gives some idea of the field’s breadth:
through an advanced understanding of animal behavior. Model systems were generalized from the study of simple and related animals to humans. For example the neuronal cortical space map discovered in bats, a specialized champion of hearing and navigating, elucidated the concept of a computational space map. In addition, the discovery of the space map in the barn owl led to the first neuronal example of the Jeffress model. This understanding is translatable to understanding spatial localization in humans, a mammalian relative of the bat. Today, knowledge learned from neuroethology are being applied in new technologies. For example, Randall Beer and his colleagues used algorithms learned from insect walking behavior to create robots designed to walk on uneven surfaces (Beer et al.). http://www.tamie.org/insect.png. Neuroethology and technology contribute to one another bidirectionally.
Neuroethologists seek to understand the neural basis of a behavior as it would occur in an animal’s natural environment but the techniques for neurophysiological analysis are lab-based, and cannot be performed in the field setting. This dichotomy between field and lab studies poses a challenge for neuroethology. From the neurophysiology perspective, experiments must be designed for controls and objective rigor, which contrasts with the ethology perspective—that the experiment be applicable to the animal’s natural condition, which is uncontrolled, or subject to the dynamics of the environment. An early example of this is when Walter Rudolf Hess developed focal brain stimulation technique to examine a cat’s brain controls of vegetative functions in addition to other behaviors. Even though this was a breakthrough in technological abilities and technique, it was not used by many neuroethologists originally because it compromised a cat’s natural state, and, therefore, in their minds, devalued the experiments' relevance to real situations.
When intellectual obstacles like this were overcome, it led to a golden age of neuroethology, by focusing on simple and robust forms of behavior, and by applying modern neurobiological methods to explore the entire chain of sensory and neural mechanisms underlying these behaviors (Zupanc 2004). New technology allows neuroethologists to attach electrodes to even very sensitive parts of an animal such as its brain while it interacts with its environment. The founders of neuroethology ushered this understanding and incorporated technology and creative experimental design. Since then even indirect technological advancements such as battery-powered and waterproofed instruments have allowed neuroethologists to mimic natural conditions in the lab while they study behaviors objectively.
In addition, the electronics required for amplifying neural signals and for transmitting them over a certain distance have enabled neuroscientists to record from behaving animals performing activities in naturalistic environments. Emerging technologies can complement neuroethology, augmenting the feasibility of this valuable perspective of natural neurophysiology.
Another challenge, and perhaps part of the beauty of neuroethology, is experimental design. The value of neuroethological criteria speak to the reliability of these experiments, because these discoveries represent behavior in the environments in which they evolved. Neuroethologists foresee future advancements through using new technologies and techniques, such as computational neuroscience, neuroendocrinology, and molecular genetics that mimic natural environments.
in the knifefish Eigenmannia sp. In collaboration with T.H. Bullock and colleagues, the behavior was further developed. Finally, the work of W. Heiligenberg
expanded it into a full neuroethology study by examining the series of neural connections that led to the behavior. Eigenmannia is a weakly electric fish that can self-generate electric discharges through electrocytes in its tail. Furthermore, it has the ability to electrolocate by analyzing the perturbations in its electric field. However when the frequency of a neighboring fish’s current is very close (less than 20 Hz difference) to that of its own, the fish will avoid having their signals interfere through a behavior known as Jamming Avoidance Response. If the neighbor’s frequency is higher than the fish’s discharge frequency, the fish will lower its frequency, and vice versa. The sign of the frequency difference is determined by analyzing the “beat” pattern of the incoming interference which consists of the combination of the two fish’s discharge patterns.
Neuroethologists performed several experiments under Eigenmannia’s natural conditions to study how it determined the sign of the frequency difference. They manipulated the fish’s discharge by injecting it with curare which prevented its natural electric organ from discharging. Then, an electrode was placed in its mouth and another was placed at the tip of its tail. Likewise, the neighboring fish’s electric field was mimicked using another set of electrodes. This experiment allowed neuroethologists to manipulate different discharge frequencies and observe the fish’s behavior. From the results, they were able to conclude that the electric field frequency, rather than an internal frequency measure, was used as a reference. This experiment is significant in that not only does it reveal a crucial neural mechanism underlying the behavior but also demonstrates the value neuroethologists place on studying animals in their natural habitats.
Ewert and coworkers adopted a variety of methods to study the predator versus prey behavior response. They conducted recording experiments where they inserted electrodes into the brain, while the toad was presented with worm or anti-worm stimuli. This technique was repeated at different levels of the visual system and also allowed feature detectors
to be identified, Video-2. In focus was the discovery of prey-selective neurons in the optic tectum, whose axons could be traced towards the snapping pattern generating cells in the hypoglossal nucleus. The discharge patterns of prey-selective tectal neurons in response to prey objects – in freely moving toads – „predicted“ prey-catching reactions such as snapping. Another approach, called stimulation experiment, was carried out in freely moving toads. Focal electrical stimuli were applied to different regions of the brain, and the toad’s response was observed. When the thalamic-pretectal region was stimulated, the toad exhibited escape responses, but when the tectum was stimulated in an area close to prey-selective neurons, the toad engaged in prey catching behavior (Carew 2000). Furthermore, neuroanatomical experiments were carried out where the toad’s thalamic-pretectal/tectal connection was lesioned and the resulting deficit noted: the prey-selective properties were abolished both in the responses of prey-selective neurons and in the prey catching behavior. These and other experiments suggest that prey selectivity results from pretecto-tectal influences, Video-3.
Ewert and coworkers showed in toads that there are stimulus-response mediating pathways that translate perception (of visual sign stimuli) into action (adequate behavioral responses). In addition there are modulatory loops that initiate, modify or specify this mediation (Ewert 2004). Regarding the latter, for example, the telencephalic caudal ventral striatum is involved in a loop gating the stimulus-response mediation in a manner of directed attention. The telencephalic ventral medial pallium („primordium hippocampi“), however, is involved in loops that either modify prey-selection due to associative learning or specify prey-selection due to non-associative learning, respectively.
is concerned with the computer modelling of animal behavior, including its underlying neural mechanisms. CN systems work within a closed-loop environment; that is, they perceive their (perhaps artificial) environment directly, rather than through human input, as is typical in AI
systems. For example, Barlow et al. developed a time-dependent model for the retina of the horseshoe crab Limulus polyphemus
on a Connection Machine
(Model CM-2). Instead of feeding the model retina with idealized input signals, they exposed the simulation to digitized video sequences made underwater, and compared its response with those of real animals.
Behavioral neuroscience
Behavioral neuroscience, also known as biological psychology, biopsychology, or psychobiology is the application of the principles of biology , to the study of physiological, genetic, and developmental mechanisms of behavior in human and non-human animals...
endeavors to understand how the central nervous system translates biologically relevant stimuli into natural behavior. For example, many bats are capable of echolocation
Animal echolocation
Echolocation, also called biosonar, is the biological sonar used by several kinds of animals.Echolocating animals emit calls out to the environment and listen to the echoes of those calls that return from various objects near them. They use these echoes to locate and identify the objects...
which is used for prey capture and navigation. The auditory system of bats is often cited as an example for how acoustic properties of sounds can be converted into a sensory map of behaviorally relevant features of sounds. Neuroethologists hope to uncover general principles of the nervous system from the study of animals with exaggerated or specialized behaviors.
As its name implies, neuroethology is a multidisciplinary field composed of neurobiology (the study of the nervous system) and ethology
Ethology
Ethology is the scientific study of animal behavior, and a sub-topic of zoology....
(the study of behavior in natural conditions). A central theme of the field of neuroethology, delineating it from other branches of neuroscience, is this focus on natural behavior. Natural behaviors may be thought of as those behaviors generated through means of natural selection
Natural selection
Natural selection is the nonrandom process by which biologic traits become either more or less common in a population as a function of differential reproduction of their bearers. It is a key mechanism of evolution....
(i.e. finding mates, navigation, locomotion, predator avoidance) rather than behaviors in disease states, or behavioral tasks that are particular to the laboratory.
Philosophy
Neuroethology is an integrative approach to solving problems in animal behavior, drawing upon several disciplines. Often, neuroethologists choose to study animals that are “specialists” in a particular type of behavior the researcher wishes to study (i.e. honeybees and their social behavior, bat echolocation, owl sound localization). The idea that an ideal animal exists for studying specific behaviors is based on Krogh's principle. The neuroethological approach stems from the idea that animals' nervous systems have evolved to address problems of sensing and acting in certain environmental niches. Central to the dogma of neuroethology, therefore, is the idea that nervous systems are best understood in the context of the problems they have evolved to solve.The scope of neuroethological inquiry might be summarized by Jörg-Peter Ewert
Jörg-Peter Ewert
Jörg-Peter Ewert is a German neurophysiologist and researcher in the field of Neuroethology. From 1973 to 2006, he served as a university professor in the Faculty of Natural Sciences at the University of Kassel, Germany.-Career:From 1958 to 1965 Jörg-Peter Ewert studied the specialties biology,...
, a pioneer of neuroethology, when he considers the types of questions central to neuroethology in his 1980 introductory text to the field:
- How are stimuli detected by an organism?
- How are environmental stimuli in the external world represented in the nervous system?
- How is information about a stimulus acquired, stored and recalled by the nervous system?
- How is a behavioral pattern encoded by neural networks?
- How is behavior coordinated and controlled by the nervous system?
- How can the ontogenetic development of behavior be related to neural mechanisms?
Often central to addressing questions in neuroethology are comparative methodologies, drawing upon knowledge about related organisms’ nervous systems, anatomies, life histories, behaviors and environmental niches. While it is not unusual for many types of neurobiology experiments to give rise to behavioral questions, many neuroethologists often begin their research programs by observing a species’ behavior in its natural environment. Other approaches to understanding nervous systems include the systems identification approach, popular in engineering
Engineering
Engineering is the discipline, art, skill and profession of acquiring and applying scientific, mathematical, economic, social, and practical knowledge, in order to design and build structures, machines, devices, systems, materials and processes that safely realize improvements to the lives of...
. The idea is to stimulate the system using a non-natural stimulus with certain properties. The system's response to the stimulus may be used to analyze the operation of the system. Such an approach is useful for linear
Linear
In mathematics, a linear map or function f is a function which satisfies the following two properties:* Additivity : f = f + f...
systems, but the nervous system is notoriously nonlinear, and neuroethologists argue that such an approach is limited. This argument is supported by experiments in the auditory system. These experiments show that neural responses to complex sounds, like social calls, can not be predicted by the knowledge gained from studying the responses due to pure tones (one of the non-natural stimuli favored by auditory neurophysiologists). This is because of the non-linearity of the system.
Modern neuroethology is largely influenced by the research techniques used. Neural approaches are necessarily very diverse, as is evident through the variety of questions asked, measuring techniques used, relationships explored, and model systems employed. Techniques utilized since 1984 include the use of intracellular dyes, which make maps of identified neurons possible, and the use of brain slices, which bring vertebrate brains into better observation through intracellular electrodes (Hoyle 1984). Currently, other fields toward which neuroethology may be headed include computational neuroscience
Computational neuroscience
Computational neuroscience is the study of brain function in terms of the information processing properties of the structures that make up the nervous system...
, molecular genetics
Molecular genetics
Molecular genetics is the field of biology and genetics that studies the structure and function of genes at a molecular level. The field studies how the genes are transferred from generation to generation. Molecular genetics employs the methods of genetics and molecular biology...
, neuroendocrinology
Neuroendocrinology
Neuroendocrinology is the study of the extensive interactions between the nervous system and the endocrine system, including the biological features of the cells that participate, and how they functionally communicate...
. The existing field of neural modeling may also expand into neuroethological terrain, due to its practical uses in robotics
Robotics
Robotics is the branch of technology that deals with the design, construction, operation, structural disposition, manufacture and application of robots...
. In all this, neuroethologists must use the right level of simplicity to effectively guide research towards accomplishing the goals of neuroethology.
Critics of neuroethology might consider it a branch of neuroscience concerned with ‘animal trivia’. Though neuroethological subjects tend not to be traditional neurobiological model systems (i.e. Drosophila
Drosophila melanogaster
Drosophila melanogaster is a species of Diptera, or the order of flies, in the family Drosophilidae. The species is known generally as the common fruit fly or vinegar fly. Starting from Charles W...
, C. elegans
Caenorhabditis elegans
Caenorhabditis elegans is a free-living, transparent nematode , about 1 mm in length, which lives in temperate soil environments. Research into the molecular and developmental biology of C. elegans was begun in 1974 by Sydney Brenner and it has since been used extensively as a model...
, or Danio rerio
Danio rerio
The zebrafish, Danio rerio, is a tropical freshwater fish belonging to the minnow family of order Cypriniformes. It is a popular aquarium fish, frequently sold under the trade name zebra danio, and is an important vertebrate model organism in scientific research.-Taxonomy:The zebrafish are...
), neuroethological approaches emphasizing comparative methods have uncovered many concepts central to neuroscience as a whole, such as lateral inhibition
Lateral inhibition
In neurobiology, lateral inhibition is the capacity of an excited neuron to reduce the activity of its neighbors. Lateral inhibition sharpens the spatial profile of excitation in response to a localized stimulus.-Sensory inhibition:...
, coincidence detection, and sensory maps
Sensory Maps
Sensory Maps are areas of the brain which respond to sensory stimulation, and are spatially organized according to some feature of the sensory stimulation. In some cases the sensory map is simply a topographic representation of a sensory surface such as the skin, cochlea, or retina...
. The discipline of neuroethology has also discovered and explained the only vertebrate behavior for which the entire neural circuit has been described: the electric fish
Electric fish
An electric fish is a fish that can generate electric fields. It is said to be electrogenic; a fish that has the ability to detect electric fields is said to be electroreceptive. Most electrogenic fish are also electroreceptive. Electric fish species can be found both in the sea and in freshwater...
jamming avoidance response
Jamming avoidance response
The jamming avoidance response or JAR is a behavior performed by some species of weakly electric fish. The JAR occurs when two electric fish with wave discharges meet – if their discharge frequencies are very similar, each fish will shift its discharge frequency to increase the difference between...
. Beyond its conceptual contributions, neuroethology makes indirect contributions to advancing human health. By understanding simpler nervous systems, many clinicians have used concepts uncovered by neuroethology and other branches of neuroscience
Neuroscience
Neuroscience is the scientific study of the nervous system. Traditionally, neuroscience has been seen as a branch of biology. However, it is currently an interdisciplinary science that collaborates with other fields such as chemistry, computer science, engineering, linguistics, mathematics,...
to develop treatments for devastating human diseases.
Historical Origins
The field of neuroethology owes part of its existence to the establishment of ethologyEthology
Ethology is the scientific study of animal behavior, and a sub-topic of zoology....
as a unique discipline within the discipline of Zoology
Zoology
Zoology |zoölogy]]), is the branch of biology that relates to the animal kingdom, including the structure, embryology, evolution, classification, habits, and distribution of all animals, both living and extinct...
. Although animal behavior had been studied since the time of Aristotle
Aristotle
Aristotle was a Greek philosopher and polymath, a student of Plato and teacher of Alexander the Great. His writings cover many subjects, including physics, metaphysics, poetry, theater, music, logic, rhetoric, linguistics, politics, government, ethics, biology, and zoology...
(384-342 BC), it was not until the early twentieth century that ethology finally became distinguished from natural science (a strictly descriptive field) and ecology. The main catalysts behind this new distinction were the research and writings of Konrad Lorenz
Konrad Lorenz
Konrad Zacharias Lorenz was an Austrian zoologist, ethologist, and ornithologist. He shared the 1973 Nobel Prize with Nikolaas Tinbergen and Karl von Frisch...
and Niko Tinbergen.
Konrad Lorenz was born in Austria in 1903, and is widely known for his contribution of the theory of fixed action pattern
Fixed action pattern
In ethology, a fixed action pattern , or modal action pattern, is an instinctive behavioral sequence that is indivisible and runs to completion...
s (FAPs): endogenous, instinctive behaviors involving a complex sequence of movements that are triggered (“released”) by a certain kind of stimulus. This sequence always proceeds to completion, even if the original stimulus is removed. It is also species-specific and performed by nearly all members. Lorenz constructed his famous “hydraulic model” to help illustrate this concept, as well as the concept of action specific energy, or drives.
Niko Tinbergen was born in the Netherlands in 1907 and worked closely with Lorenz in the development of the FAP theory; their studies focused on the egg retrieval response of nesting geese. Tinbergen performed extensive research on the releasing mechanisms of particular FAPs, and used the bill-pecking behavior of baby herring gulls as his model system. This led to the concept of the supernormal stimulus. Tinbergen is also well known for his four questions
Tinbergen's four questions
Tinbergen's four questions, named after Nikolaas Tinbergen, are complementary categories of explanations for behavior. It suggests that an integrative understanding of behavior must include both a proximate and ultimate analysis of behavior, as well as an understanding of both...
that he believed ethologists should be asking about any given animal behavior; among these is that of the mechanism of the behavior, on a physiological, neural and molecular level, and this question can be thought of in many regards as the keystone question in neuroethology. Tinbergen also emphasized the need for ethologists and neurophysiologists to work together in their studies, a unity that has become a reality in the field of neuroethology.
Unlike behaviorism
Behaviorism
Behaviorism , also called the learning perspective , is a philosophy of psychology based on the proposition that all things that organisms do—including acting, thinking, and feeling—can and should be regarded as behaviors, and that psychological disorders are best treated by altering behavior...
, which studied animals' reactions to non-natural stimuli
Stimulus (physiology)
In physiology, a stimulus is a detectable change in the internal or external environment. The ability of an organism or organ to respond to external stimuli is called sensitivity....
in artificial, laboratory
Laboratory
A laboratory is a facility that provides controlled conditions in which scientific research, experiments, and measurement may be performed. The title of laboratory is also used for certain other facilities where the processes or equipment used are similar to those in scientific laboratories...
conditions, ethology sought to categorize and analyze the natural behaviors of animals in a field setting. Similarly, neuroethology asks questions about the neural bases of naturally occurring behaviors, and seeks to mimic the natural context as much as possible in the laboratory.
Although the development of ethology as a distinct discipline was crucial to the advent of neuroethology, equally important was the development of a more comprehensive understanding of Neuroscience
Neuroscience
Neuroscience is the scientific study of the nervous system. Traditionally, neuroscience has been seen as a branch of biology. However, it is currently an interdisciplinary science that collaborates with other fields such as chemistry, computer science, engineering, linguistics, mathematics,...
. Contributors to this new understanding were the Spanish Neuroanatomist, Ramon y Cajal (born in 1852), and physiologists Charles Sherrington, Edgar Adrian, Alan Hodgkin, and Andrew Huxley
Andrew Huxley
Sir Andrew Fielding Huxley, OM, FRS is an English physiologist and biophysicist, who won the 1963 Nobel Prize in Physiology or Medicine for his experimental and mathematical work with Sir Alan Lloyd Hodgkin on the basis of nerve action potentials, the electrical impulses that enable the activity...
. Charles Sherrington, who was born in Great Britain in 1857, is famous for his work on the nerve synapse as the site of transmission of nerve impulses, and for his work on reflexes in the spinal cord. His research also led him to hypothesize that every muscular activation is coupled to an inhibition of the opposing muscle. He was awarded a Nobel Prize for his work in 1932 along with Lord Edgar Adrian who made the first physiological recordings of neural activity from single nerve fibers.
Alan Hodgkin and Andrew Huxley
Andrew Huxley
Sir Andrew Fielding Huxley, OM, FRS is an English physiologist and biophysicist, who won the 1963 Nobel Prize in Physiology or Medicine for his experimental and mathematical work with Sir Alan Lloyd Hodgkin on the basis of nerve action potentials, the electrical impulses that enable the activity...
(born 1914 and 1917, respectively, in Great Britain), are known for their collaborative effort to understand the production of action potentials in giant squid neurons. The pair also proposed the existence of ion channels to facilitate action potential initiation, and were awarded the Nobel Prize in 1963 for their efforts.
As a result of this pioneering research, many scientists then sought to connect the physiological aspects of the nervous and sensory systems to specific behaviors. These scientists – Karl von Frisch
Karl von Frisch
Karl Ritter von Frisch was an Austrian ethologist who received the Nobel Prize in Physiology or Medicine in 1973, along with Nikolaas Tinbergen and Konrad Lorenz....
, Erich von Holst
Erich von Holst
Erich von Holst , was a German behavioral physiologist who was a native of Riga, and was related to historian Hermann Eduard von Holst...
, and Theodore Bullock – are frequently referred to as the “fathers” of neuroethology. Neuroethology did not really come into its own, though, until the 1970s and 1980s, when new, sophisticated experimental methods allowed researchers such as Masakazu Konishi
Masakazu Konishi
is a Japanese neurobiologist, known for his research on prey capture auditory systems of barn owls and singing in songbirds.-Life:After growing up in wartime Kyoto, Konishi moved to study at Sapporo Agricultural College, Hokkaido University. Konishi studied for his doctoral thesis on properties of...
, Walter Heiligenberg
Walter Heiligenberg
Walter Heiligenberg is best known for his contribution to neuroethology through his work on one of the best neurologically understood behavioral patterns in vertebrate, Eigenmannia...
, Jörg-Peter Ewert
Jörg-Peter Ewert
Jörg-Peter Ewert is a German neurophysiologist and researcher in the field of Neuroethology. From 1973 to 2006, he served as a university professor in the Faculty of Natural Sciences at the University of Kassel, Germany.-Career:From 1958 to 1965 Jörg-Peter Ewert studied the specialties biology,...
, and others to study the neural circuits underlying verifiable behavior.
Modern neuroethology
The International Society for Neuroethology (ISN) represents the present discipline of neuroethology, which was founded on the occasion of the NATO-Advanced Study Institute "Advances in Vertebrate Neuroethology" (August 13–24, 1981) organized by J.-P. Ewert, D.J. Ingle and R.R. Capranica, held at the University of Kassel in Hofgeismar, Germany (cf. report Trends in Neurosci. 5:141-143,1982). The first president of ISN was Theodore H. Bullock. The ISN has met every three years since its first meeting in Tokyo in 1986.Its membership draws from many research programs around the world; many of its members are students and faculty members from medical schools and neurobiology departments from various universities. Modern advances in neurophysiology
Neurophysiology
Neurophysiology is a part of physiology. Neurophysiology is the study of nervous system function...
techniques have enabled more exacting approaches in an ever-increasing number of animal systems, as size limitations are being dramatically overcome. Survey of the most recent (2007) congress of the ISN meeting symposia topics gives some idea of the field’s breadth:
- Comparative aspects of spatial memory (rodents, birds, humans, bats)
- Influences of higher processing centers in active sensing (primates, owls, electric fish, rodents, frogs)
- Animal signaling plasticity over many time scales (electric fish, frogs, birds)
- Song production and learning in passerine birds
- Primate sociality
- Optimal function of sensory systems (flies, moths, frogs, fish)
- Neuronal complexity in behavior (insects, computational)
- Contributions of genes to behavior (Drosophila, honeybees, zebrafish)
- Eye and head movement (crustaceans, humans, robots)
- Hormonal actions in brain and behavior (rodents, primates, fish, frogs, and birds)
- Cognition in insects (honeybee)
Application to technology
Neuroethology can help create advancements in technologyTechnology
Technology is the making, usage, and knowledge of tools, machines, techniques, crafts, systems or methods of organization in order to solve a problem or perform a specific function. It can also refer to the collection of such tools, machinery, and procedures. The word technology comes ;...
through an advanced understanding of animal behavior. Model systems were generalized from the study of simple and related animals to humans. For example the neuronal cortical space map discovered in bats, a specialized champion of hearing and navigating, elucidated the concept of a computational space map. In addition, the discovery of the space map in the barn owl led to the first neuronal example of the Jeffress model. This understanding is translatable to understanding spatial localization in humans, a mammalian relative of the bat. Today, knowledge learned from neuroethology are being applied in new technologies. For example, Randall Beer and his colleagues used algorithms learned from insect walking behavior to create robots designed to walk on uneven surfaces (Beer et al.). http://www.tamie.org/insect.png. Neuroethology and technology contribute to one another bidirectionally.
Neuroethologists seek to understand the neural basis of a behavior as it would occur in an animal’s natural environment but the techniques for neurophysiological analysis are lab-based, and cannot be performed in the field setting. This dichotomy between field and lab studies poses a challenge for neuroethology. From the neurophysiology perspective, experiments must be designed for controls and objective rigor, which contrasts with the ethology perspective—that the experiment be applicable to the animal’s natural condition, which is uncontrolled, or subject to the dynamics of the environment. An early example of this is when Walter Rudolf Hess developed focal brain stimulation technique to examine a cat’s brain controls of vegetative functions in addition to other behaviors. Even though this was a breakthrough in technological abilities and technique, it was not used by many neuroethologists originally because it compromised a cat’s natural state, and, therefore, in their minds, devalued the experiments' relevance to real situations.
When intellectual obstacles like this were overcome, it led to a golden age of neuroethology, by focusing on simple and robust forms of behavior, and by applying modern neurobiological methods to explore the entire chain of sensory and neural mechanisms underlying these behaviors (Zupanc 2004). New technology allows neuroethologists to attach electrodes to even very sensitive parts of an animal such as its brain while it interacts with its environment. The founders of neuroethology ushered this understanding and incorporated technology and creative experimental design. Since then even indirect technological advancements such as battery-powered and waterproofed instruments have allowed neuroethologists to mimic natural conditions in the lab while they study behaviors objectively.
In addition, the electronics required for amplifying neural signals and for transmitting them over a certain distance have enabled neuroscientists to record from behaving animals performing activities in naturalistic environments. Emerging technologies can complement neuroethology, augmenting the feasibility of this valuable perspective of natural neurophysiology.
Another challenge, and perhaps part of the beauty of neuroethology, is experimental design. The value of neuroethological criteria speak to the reliability of these experiments, because these discoveries represent behavior in the environments in which they evolved. Neuroethologists foresee future advancements through using new technologies and techniques, such as computational neuroscience, neuroendocrinology, and molecular genetics that mimic natural environments.
Jamming avoidance response
In 1963, two scientists, Akira Watanabe and Kimihisa Takeda, discovered the behavior of the jamming avoidance responseJamming avoidance response
The jamming avoidance response or JAR is a behavior performed by some species of weakly electric fish. The JAR occurs when two electric fish with wave discharges meet – if their discharge frequencies are very similar, each fish will shift its discharge frequency to increase the difference between...
in the knifefish Eigenmannia sp. In collaboration with T.H. Bullock and colleagues, the behavior was further developed. Finally, the work of W. Heiligenberg
Walter Heiligenberg
Walter Heiligenberg is best known for his contribution to neuroethology through his work on one of the best neurologically understood behavioral patterns in vertebrate, Eigenmannia...
expanded it into a full neuroethology study by examining the series of neural connections that led to the behavior. Eigenmannia is a weakly electric fish that can self-generate electric discharges through electrocytes in its tail. Furthermore, it has the ability to electrolocate by analyzing the perturbations in its electric field. However when the frequency of a neighboring fish’s current is very close (less than 20 Hz difference) to that of its own, the fish will avoid having their signals interfere through a behavior known as Jamming Avoidance Response. If the neighbor’s frequency is higher than the fish’s discharge frequency, the fish will lower its frequency, and vice versa. The sign of the frequency difference is determined by analyzing the “beat” pattern of the incoming interference which consists of the combination of the two fish’s discharge patterns.
Neuroethologists performed several experiments under Eigenmannia’s natural conditions to study how it determined the sign of the frequency difference. They manipulated the fish’s discharge by injecting it with curare which prevented its natural electric organ from discharging. Then, an electrode was placed in its mouth and another was placed at the tip of its tail. Likewise, the neighboring fish’s electric field was mimicked using another set of electrodes. This experiment allowed neuroethologists to manipulate different discharge frequencies and observe the fish’s behavior. From the results, they were able to conclude that the electric field frequency, rather than an internal frequency measure, was used as a reference. This experiment is significant in that not only does it reveal a crucial neural mechanism underlying the behavior but also demonstrates the value neuroethologists place on studying animals in their natural habitats.
Feature analysis in toad vision
The recognition of prey and predators in the toad was first studied in depth by Jörg-Peter Ewert (Ewert 1974; see also 2004). He began by observing the natural prey-catching behavior of the common toad (Bufo bufo) and concluded that the animal followed a sequence that consisted of stalking, binocular fixation, snapping, swallowing and mouth-wiping. However, initially, the toad’s actions were dependent on specific features of the sensory stimulus: whether it demonstrated worm or anti-worm configurations, see Video. It was observed that the worm configuration, which signaled prey, was initiated by movement along the object's long axis, whereas anti-worm configuration, which signaled predator, was due to movement along the short axis, Video-1 (Zupanc 2004).Ewert and coworkers adopted a variety of methods to study the predator versus prey behavior response. They conducted recording experiments where they inserted electrodes into the brain, while the toad was presented with worm or anti-worm stimuli. This technique was repeated at different levels of the visual system and also allowed feature detectors
Feature detection
In computer vision and image processing the concept of feature detection refers to methods that aim at computing abstractions of image information and making local decisions at every image point whether there is an image feature of a given type at that point or not...
to be identified, Video-2. In focus was the discovery of prey-selective neurons in the optic tectum, whose axons could be traced towards the snapping pattern generating cells in the hypoglossal nucleus. The discharge patterns of prey-selective tectal neurons in response to prey objects – in freely moving toads – „predicted“ prey-catching reactions such as snapping. Another approach, called stimulation experiment, was carried out in freely moving toads. Focal electrical stimuli were applied to different regions of the brain, and the toad’s response was observed. When the thalamic-pretectal region was stimulated, the toad exhibited escape responses, but when the tectum was stimulated in an area close to prey-selective neurons, the toad engaged in prey catching behavior (Carew 2000). Furthermore, neuroanatomical experiments were carried out where the toad’s thalamic-pretectal/tectal connection was lesioned and the resulting deficit noted: the prey-selective properties were abolished both in the responses of prey-selective neurons and in the prey catching behavior. These and other experiments suggest that prey selectivity results from pretecto-tectal influences, Video-3.
Ewert and coworkers showed in toads that there are stimulus-response mediating pathways that translate perception (of visual sign stimuli) into action (adequate behavioral responses). In addition there are modulatory loops that initiate, modify or specify this mediation (Ewert 2004). Regarding the latter, for example, the telencephalic caudal ventral striatum is involved in a loop gating the stimulus-response mediation in a manner of directed attention. The telencephalic ventral medial pallium („primordium hippocampi“), however, is involved in loops that either modify prey-selection due to associative learning or specify prey-selection due to non-associative learning, respectively.
Computational neuroethology
Computational neuroethology (CN or CNE)is concerned with the computer modelling of animal behavior, including its underlying neural mechanisms. CN systems work within a closed-loop environment; that is, they perceive their (perhaps artificial) environment directly, rather than through human input, as is typical in AI
Artificial intelligence
Artificial intelligence is the intelligence of machines and the branch of computer science that aims to create it. AI textbooks define the field as "the study and design of intelligent agents" where an intelligent agent is a system that perceives its environment and takes actions that maximize its...
systems. For example, Barlow et al. developed a time-dependent model for the retina of the horseshoe crab Limulus polyphemus
Horseshoe crab
The Atlantic horseshoe crab, Limulus polyphemus, is a marine chelicerate arthropod. Despite its name, it is more closely related to spiders, ticks, and scorpions than to crabs. Horseshoe crabs are most commonly found in the Gulf of Mexico and along the northern Atlantic coast of North America...
on a Connection Machine
Connection Machine
The Connection Machine was a series of supercomputers that grew out of Danny Hillis' research in the early 1980s at MIT on alternatives to the traditional von Neumann architecture of computation...
(Model CM-2). Instead of feeding the model retina with idealized input signals, they exposed the simulation to digitized video sequences made underwater, and compared its response with those of real animals.
Model systems
- Bat echolocation – nocturnal flight navigation and prey capture; location of objects using echo returns of its own call
- OscineSongbirdA songbird is a bird belonging to the suborder Passeri of the perching birds . Another name that is sometimes seen as scientific or vernacular name is Oscines, from Latin oscen, "a songbird"...
bird songBird songBird vocalization includes both bird calls and bird songs. In non-technical use, bird songs are the bird sounds that are melodious to the human ear. In ornithology and birding, songs are distinguished by function from calls.-Definition:The distinction between songs and calls is based upon...
– Zebra Finch (Taeniopygia guttata), Canary (Serinus canaria) and White-crowned Sparrow (Zonotrichia leucophrys); song learning as a model for human speech development - Electric fishElectric fishAn electric fish is a fish that can generate electric fields. It is said to be electrogenic; a fish that has the ability to detect electric fields is said to be electroreceptive. Most electrogenic fish are also electroreceptive. Electric fish species can be found both in the sea and in freshwater...
– navigation, communication, Jamming Avoidance Response (JAR), corollary dischargePID controllerA proportional–integral–derivative controller is a generic control loop feedback mechanism widely used in industrial control systems – a PID is the most commonly used feedback controller. A PID controller calculates an "error" value as the difference between a measured process variable and a...
, expectation generators, and spike timing dependent plasticity - Barn OwlBarn OwlThe Barn Owl is the most widely distributed species of owl, and one of the most widespread of all birds. It is also referred to as Common Barn Owl, to distinguish it from other species in the barn-owl family Tytonidae. These form one of two main lineages of living owls, the other being the typical...
auditory spatial map – nocturnal prey location and capture - Toad visionVision in toadsThe neural basis of prey detection, recognition, and orientation was studied in depth by Jörg-Peter Ewert in a series of experiments that made the toad visual system a model system in neuroethology...
– discrimination of prey versus predator --Video „Image processing in the toad’s visual system: behavior, brain function, artificial neuronal net“ - Cricket song – mate attraction and corollary discharge
- Fish Mauthner cells – C-start escape response and underwater directional hearing
- Fly – Microscale directional hearing in OrmiaOrmiaOrmia is a small genus of nocturnal flies in the family Tachinidae, that are parasites of crickets. The genus occurs throughout the Americas....
ochracea, sex differences of the visual systemSex differences in sensory systemsAn organism is said to be sexually dimorphic when male and female conspecifics have anatomical differences in features such as body size, coloration, or ornamentation, but disregarding differences of reproductive organs. Sexual dimorphism is usually a product of sexual selection, with female choice...
in BibionidaeBibionidaeBibionidae is a family of flies . Approximately 650-700 species are known worldwide.-Biology:...
, and spatial navigation in chasing behavior of Fannia canicularis - Noctuid moths – ultrasound avoidanceUltrasound avoidanceUltrasound avoidance is an escape or avoidance reflex displayed by certain animal species that are preyed upon by echolocating predators. Ultrasound avoidance is known for several groups of insects that have independently evolved mechanisms for ultrasonic hearing...
response to bat calls - AplysiaAplysiaAplysia is a genus of medium-sized to extremely large sea slugs, specifically sea hares, which are one clade of large sea slugs, marine gastropod mollusks. The general description of sea hares can be found in the article on the superfamily Aplysioidea....
– learning and memory in startle response - Rat – spatial memorySpatial memoryIn cognitive psychology and neuroscience, spatial memory is the part of memory responsible for recording information about one's environment and its spatial orientation. For example, a person's spatial memory is required in order to navigate around a familiar city, just as a rat's spatial memory is...
and navigation - Salmon homingHoming (biology)Homing is the inherent ability of an animal to navigate towards an original location through unfamiliar areas. This location may be either a home territory, or a breeding spot.-Uses:...
– olfactory imprinting and thyroid hormoneThyroid hormoneThe thyroid hormones, thyroxine and triiodothyronine , are tyrosine-based hormones produced by the thyroid gland primarily responsible for regulation of metabolism. An important component in the synthesis of thyroid hormones is iodine. The major form of thyroid hormone in the blood is thyroxine ,...
s - CrayfishCrayfishCrayfish, crawfish, or crawdads – members of the superfamilies Astacoidea and Parastacoidea – are freshwater crustaceans resembling small lobsters, to which they are related...
– escape and startle behaviors, aggression and formation of social hierarchies - CichlidCichlidCichlids are fishes from the family Cichlidae in the order Perciformes. Cichlids are members of a group known as the Labroidei along with the wrasses , damselfish , and surfperches . This family is both large and diverse. At least 1,300 species have been scientifically described, making it one of...
fish – aggression and attack behaviors - Honey beeHoney beeHoney bees are a subset of bees in the genus Apis, primarily distinguished by the production and storage of honey and the construction of perennial, colonial nests out of wax. Honey bees are the only extant members of the tribe Apini, all in the genus Apis...
– learning, navigation, vision, olfaction, flight, aggression, foraging - More Model Systems and Information
Textbooks
- Zupanc, G.K.H. (2004) Behavioral Neurobiology an Integrative Approach. Oxford University Press, New York.
- Carew, T.J. (2000) Behavioral Neurobiology: The Cellular Organization of Natural Behavior. Sinauer, Sunderland Mass.
- Simmons, P., Young, D. (1999) Nerve Cells and Animal Behaviour. Second Edition. Cambridge University Press, New York.
- Simmons, P., Young, D. (2010) Nerve Cells and Animal Behaviour. Third Edition. Cambridge University Press, New York.
- Camhi J. (1984) Neuroethology: Nerve Cells and the Natural Behavior of Animals. Sinauer Associates, Sunderland Mass.
- Guthrie, D.M. (1980) Neuroethology: An Introduction. Wiley, New York.
- Ewert, J.-P. (1980) Neuroethology: An Introduction to the Neurophysiological Fundamentals of Behaviour. Springer-Verlag, New York.
- Ewert, J.-P. (1976) Neuroethologie: Einführung in die neurophysiologischen Grundlagen des Verhaltens. HT 181. Springer-Verlag Heidelberg, Berlin, New York.
- Kandel, E.R. (1976) Cellular Basis of Behavior: An Introduction to Behavioral Neurobiology. W.H. Freeman
- Roeder, K.D. (1967) Nerve Cells and Insect Behavior. Harvard University Press, Cambridge Mass.
- Marler, P., Hamilton, W.J. (1966) Mechanisms of Animal Behavior. John Wiley & Sons Inc., New York.
See also
- Niko Tinbergen
- Karl von FrischKarl von FrischKarl Ritter von Frisch was an Austrian ethologist who received the Nobel Prize in Physiology or Medicine in 1973, along with Nikolaas Tinbergen and Konrad Lorenz....
- Konrad LorenzKonrad LorenzKonrad Zacharias Lorenz was an Austrian zoologist, ethologist, and ornithologist. He shared the 1973 Nobel Prize with Nikolaas Tinbergen and Karl von Frisch...
- Erich von HolstErich von HolstErich von Holst , was a German behavioral physiologist who was a native of Riga, and was related to historian Hermann Eduard von Holst...
- Theodore H. Bullock
- Jörg-Peter EwertJörg-Peter EwertJörg-Peter Ewert is a German neurophysiologist and researcher in the field of Neuroethology. From 1973 to 2006, he served as a university professor in the Faculty of Natural Sciences at the University of Kassel, Germany.-Career:From 1958 to 1965 Jörg-Peter Ewert studied the specialties biology,...
- Eric KnudsenEric KnudsenEric Knudsen is a professor of neurobiology at Stanford University. He is best known for his discovery, along with Masakazu Konishi, of a brain map of sound location in two dimensions in the barn owl, tyto alba...
- Masakazu KonishiMasakazu Konishiis a Japanese neurobiologist, known for his research on prey capture auditory systems of barn owls and singing in songbirds.-Life:After growing up in wartime Kyoto, Konishi moved to study at Sapporo Agricultural College, Hokkaido University. Konishi studied for his doctoral thesis on properties of...
External links
- International Society for Neuroethology
- Topics in Neuroethology
- http://www.tamie.org/insect.png