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The Scope of Neuroethology

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The Scope of Neuroethology THE BEHAVIORAL AND BRAIN SCIENCES (1984) 7, 367-412 Printed in the United States of America The scope of neuroethology Graham Hoyle Institute of Neuroscience, University of Oregon, Eugene, Oreg. 97403 Abstract: Neuroethology, an interdisciplinary subdivision of neuroscience, has emerged in recent years. Since 1976 there has been a regular session under this heading at the annual meeting of the Society for Neuroscience. In 1980 two introductory texts in English were published on the subject (Ewert 1980; Guthrie 1980), and a third (Camhi 1984) was published recently. There is widespread interest in neural mechanisms underlying behavior, but they encompass such a vast array of often unrelated topics that proponents do not share common goals. This article describes the emergence of ethology as a discipline, pointing out that its practitioners were successful because they confined their research to stereotyped, complex, nonlearned, innate behavioral acts. A limited number of profoundly significant principles emerged. Each of these is redefined. The major concepts of earlier ethology were embodied in a simple hydraulic model used by Konrad Lorenz in 1949 (Lorenz 1950). It is pointed out that this model implies the existence of common neurophysiological mechanisms and neuronal circuitry. This model has now been made obsolete by neurophysiological progress, but with appropriate ~nodificationsan updated version may still be useful in focusing attention on possible principles. The initial aim of neuroethology should be to examine the neurophysiological events in a variety of behaviors, exhibited by diverse animals from different phyla, which meet the criteria of innate behavioral acts. The behaviors should be sufficiently complex to interest ethologists, yet they should be addressable with neurophysiological methods down to the cellular level. In the case of vertebrates this may mean working with brain slices as well as whole animals, but for some invertebrates recording should be possible in the nearly intact animal duringexecution ofthe behavior. The work will be exacting and very difficult, and it is not likely toget done at all unless neuroethologists recognize that they should both train and discipline themselves and restrict their attention to well- defined goals. Keywords: behavioral biology; behavior patterns; ethology; fixed action patterns (FAPs);instinct; learning; Lorcnz; lnotor programs; neuroethology Historical origins of ethology experimental investigations into the possible functional relations of a nervous system to behavior were undoubt- A scientific discipline of neuroethology could not have edly those of Galen made 1,800 years ago. There is a existed either before the term "ethology" had become direct line from his unparalleled starts, through the ideas established or before neuroscience had developed to the of Descartes and the experiments of Francis Glisson and point where both neuroanatomical and neurophysiologi- Albrecht Haller, via Charles Bell and Francois Magen- cal methods were available that could be used to attack die, to those of Johannes Miiller and his pupil Emil du ethological questions. There is a strong tendency to Bois-Reymond, who can be considered to have founded . equate neuroethology with the neural bases of behavior modern experimental neuroscience. Spice the above in the broadest sense. To do so encompasses such a broad with some Galvani, Hall, Helmholtz, Weber and Bern- spectrum of phenomena that the extremes are virtually stein; then mix with some Gall (no pun intended), unrelated and can only be linked by the widest stretches Fechner, Wundt and Titchener, and finally, a liberal dash of imagination. Such links are too tenuous. If the term of Pavlov and Sherrington, bake, cool, then top offwith an "neuroethology" is to serve the useful purpose of identi- icing of Cajal and Golgi, and you have neuroscience cake. fying a group of active scholar-investigators sharing com- The point is that here we have the product of the mon goals, to bring them together and stimulate their combined histories of much of physiology, medical neu- research, it must be relatively narrowly defined. There roanatomy, and psychophysics. But still this was not are clearly dangers in defining any subject too narrowly, nearly enough to provide a satisfactory basis for the because this can lead to the arbitrary exclusion from understanding of behavior, although in many circles, serious consideration ofinformation, especially of that yet especially Russian and British ones, it was considered to be discovered, that is truly relevant and significant for more than adequate. Even a generation of American the mainstream. But the danger is much less than that pioneers in the study of behavior, Whitman (1819), Craig associated with using a definition that is too broad. Unless (1918), McDougall (1923), Russell (1934) and eventually the focus is restricted, the subject matter expands into a B. F. Skinner [see special issue on the work of B. F. diffuse vapor without any substance at all. Skinner, BBS 7(4) 19841, had failed to realize that some- The first potential trap is to assume that the term is thing important had been left out. Fortunately, careful merely a faddish one, culled to draw attention to a and systematic examination of examples of the behavior, previously nameless but ancient line of inquiry. The first in natural rather than laboratory settings, of a variety of 6 1984 Cambridae Univenitv Press 0140-525Xl84IO30367-46/%06.00 Hoyle: Neuroethology animal species, especially of relatively lowly forms in- his book was published in 1951. He referred to The Study cluding invertebrates (though mainly insects), enabled a of Instinct as a "programme for ethology" in spite of the group of Middle-European zoologists to detect some very title. important missing ingredients in the mixture. The word "instinct" is derived from the Latin in- For the animal kingdom as a whole, the majority of stinctus, past participle of instinguere. The origin of this even the most complex behaviors, the ones with the word was associated with the use ofa pointed stick, and it longest sequences of coordinated movements and the can mean "to prick." Instinctus, as used by Cicero, is to subtlest interactions with other individuals of the same be incited, or fired up - doubtless equivalent to the species, fall into the category of instinctive acts. They responses engendered by being jabbed. This is very require no experience of the behavior in its context, nor clearly a reflex action. Paradoxically, that is not what learning, for their perfect execution. Such behavioral Lorenz wanted to convey. The whole "point" of the sequences can be broken down into a few discrete coinpo- ethological movement was that it uncovered a multitude nents. each a distinct act or subroutine. Some of the acts of common behaviors that are not akin to reflexes. even could be recognized as also being performed by related, when triggering is involved. To emphasize the difference but different, species in which they occurred in a differ- ethologists sometimes referred to the behavior as "en- ent sequence. In a few instances it has been possible to dogenous" - generated from within. A reflex will occur at show that Mendelian laws apply to the inheritance of the all times unless it is either habituated or centrallv SUD- ability to perform these acts. pressed during the execution of other behavior. An in- The realization that there is genetic involvement with stinctive behavior will occur only when there is a central chunks of behavior provided a major breakthrough in the nervous system readiness. Lorenz termed this the "ac- understanding of how complex behaviors have evolved. tion specific energy" for that particular behavior. Thorpe Natural selection clearly acts on the totality of the behav- (1979) and others have done ethology a disservice by ior. But at some evolutionary stage, what eventually erroneously attributing to Lorenz the designation "reac- became a subroutine must have been a complete behav- tion specific energy," which connotes reflex action. ior. Possiblv an entire subroutine can a~~earas a muta - Lorenz thought in terms of a gradual accumulation of a tion and become incorporated in a sequk;lce if it confers "reservoir ofuenergy" for the bLhavior in question, which selective advantage. But in spite of the simplicity and must be full, or nearly so, or the behavior will not occur at fundamental importance of these findings, they sank into all. But no catchy word or phrase has yet been coined that the minds of a majority of both behavioral scientists and adequately conveys the endogenous aspect. Since the physiologists very slowly. In fact, it was not until the 1973 success of the Lorenz-Tinbergen studies, the term Nobel Prize for physiology or medicine was awarded to instinct has come to be used differently from the way it Konrad Lorenz, Niko Tinbergen, and Karl von Frisch for was formerly, and it now carries with it the implication of their pioneering studies in these aspects of behavior that at least partially endogenous generation. he aspect of the majority of psychologists and biologists interested in releasability and the implication of spontaneous ap- behavior even accorded the work any attention. When pearance were, even in Roman times, associated with the the news broke in the United States, it did not receive the word instinctus. Those were times when emperors, in customarv, . laudi its associated with Nobel ~rizean - ~articular.used to "flv off the handle." nouncements in most of the relevant quarters. Quite the In Germany, there had been a move toward a scienceof contrary! While the furor.was still raging, students of neuroethology in Erich von Holst's Max Planck laborato- animal behavior were crowding libraries trying to find out ry of Verhaltensphysiologie (founded at Seewiesen, what these "unknowns" had discovered; indeed - what where Lorenz already had an Abteilung); this laboratory was the fuss all about? Details may be found in a fascinat- nurtured cybernetics pioneer Horst ~ittlestaedt.But this ing historical account by Thorpe (1979).
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