Graham Hoyle

The scope of neuroethology

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 ~nodifications an 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.

Cellular Mechanisms Underlying Behavior—Neuroethology

Publisher Summary There are many attractions in principle to the use of insects in the study of neural mechanisms underlying behavior-availability, simplicity of neural organization, small numbers of nerve cells, short life cycle, and so forth. Because insects are largely terrestrial and have invaded a very wide variety of environments, they have also evolved many complex behavior patterns. Instinctive behavior is not at all well understood in higher animals, nor is the mechanism of learning, and they must eventually be understood at the cellular level before real progress in neurophysiological understanding of behavior can be achieved. Both have been amply demonstrated to occur in a number of insects and, therefore, insects might be able to play a significant role in fundamental studies on them, just as did Drosophila in genetics. The problem is that research in insect neurobiology proceeds by happenstance, not plan; the whims of investigators, current fashions, and the influence of immediate “key” figures, guide an army consisting entirely of captains—no men, no generals. The most-investigated insect, both neurophysiologically and otherwise, at the present time, is the locust Schistocerca gregaria. Comparable experiments in the case of terrestrial insects are being attempted in the study of locomotion, both of flight and walking, and of singing in crickets. The extent to which these experiments are being successful is considered in this chapter.

Neuronal Network Triggering a Fixed Action Pattern

Bursts of impulses in groups of brain cells of the nudibranch Tritonia trigger prolonged swimming that is identical to the natural escape response. The cells in which the activity occurs form two bilaterally symmetrical groups of at least 30 cells in each pleural ganglion. These neurons are interconnected by pathways that have a low electrical resistance, both within a ganglion and across the brain. Together they form a network that determinies whether a swimming escape response will occur or not by filtering out weak neural activity yet responding with a burst of impulses to intensive specific input to either group.

NEUROMUSCULAR PHYSIOLOGY OF GIANT MUSCLE FIBERS OF A BARNACLE, BALANUS NUBILUS DARWIN.

Abstract 1. 1. The large barnacle, Balanus nubilis , contains several large muscles, all of which contain cross striated muscle fibers of great thickness. In large specimens single fibers over 2 mm thick have been found. 2. 2. The fibers receive innervation from two or three motor axons. 3. 3. The axons give post-synaptic potentials of small or larger size. The small post-synaptic potentials do not reach the threshold for eliciting a graded response; the larger ones do. The corresponding mechanical responses which are elicited are very small or moderate-sized twitches. 4. 4. The giant fibers give large resting potentials which are stable over long periods. The fibers contract strongly when stimulated. It is considered that this will be a valuable preparation for the study of fundamental aspects of nerve-muscle physiology.

Giant Muscle Fibers in a Barnacle, Balanus nubilus Darwin

Cross-striated muscle fibers of very large size have been found in the scutal-tergal adductor and depressor muscles of the large barnacle B. nubilus. Adductor muscle fibers are up to 2 mm thick. They are innervated by separate nerves, each supplying one end, but not the central region, with terminals; each fiber receives two or three excitor axons. Depressor muscle fibers are up to 1.4 mm thick and receive multiterminal innervation along their entire length; they are innervated by two excitor axons. Postsynaptic potentials are of small or large size and lead to small or large twitches; they do not show facilitation. The muscle fibers shorten to as little as one-sixth resting length.

Nature of the Excitatory Sarcoplasmic Reticular Junction

The appositional regions between the surface membrane and sarcoplasmic reticulum in insects, decapod crustaceans, and barnacles are largely diadic and show a four-layered structure which is roughly circular in surface view. Each consists of the 56-angstrom double-membrane of the in-termediary (here called excitatory) element, and the 75-� double-membrane of the cisternal element of the reticulum, separated by a space of about 100 �. A sheet of electron-dense material is found between the two elements, giving the superficial appearance of an additional membrane. The orbits of thin filaments around the thick filaments adjacent to both excitatory and reticular elements are incomplete on the contact side. Regularly spaced bridges connect the thick filaments with both the excitatory elements and cisternal elements and hold the diads in place during stretch and contraction.

On the Way to Neuroethology: The Identified Neuron Approach

The late Kenneth Roeder, whom I had the pleasure of first meeting in 1955, and many times thereafter, was a major source of inspiration. He was singular, for the late 1930’s, in realizing the potential insects offer for a deep understanding of how nerve cells generate and of control behavior. I think the only other person to perceive this potential may have been V.B. Wigglesworth, but Sir. Vincent hated complex instruments, especially cathode-ray oscillographs, and he positively went out of his way to avoid contact with both them and their “slaves”, as he felt insect neuroscientists soon became. By contrast, Roeder manifestly enjoyed playing with oscilloscopes and looking at spikes. Following his retirement, when he was often too ill to travel to his Tufts University laboratory, Roeder would be busy in his garage. There, his devoted students had helped him set up an excellent neurorecording rig. But first and foremost he was a naturalist who loved the subtleties of animal behavior. He felt that his first call was to the whole animal, so he never made a total commitment to neuroscience as a discipline. I think he was afraid of getting lost in what he perceived as the narrow, though seductive, world of biophysics. For him, communication with intercellular neuronal traffic via extracellular action potentials provided ample food for a lively mind. And of course, he wonderfully illuminated our understanding of insect life by his skillful, perceptive probings.

Cellular Basis of Operant-Conditioning of Leg Position

Leg position learning is accomplished rapidly and successfully by insect thoracic ganglia in operant-conditioning paradigms using either negative or positive reinforcements. This opens up the possibility of analysis of the cellular mechanisms underlying learning and retention because the neurons are relatively few in number, identifiable and repeatedly addressable. Starting with positions controlled by single identified motorneurons we find that these are changed in relation to reinforcement either by very long-lasting frequency shifts or by adjustment of the strength and repetition interval of spontaneously-occurring plateau movements, depending on the paradigm. Postural change is accomplished by altered resistance of a motorneuron, specifically associated with potassium conductance. The resistance range is from 3–10 M Ω , with associated mean frequency range of 5–30 Hz. Only goal-related inputs lead to postural shifts, by way of association of reinforcement with efference or afference memory.

Learning of leg position by the ghost crab Ocypode ceratophthalma

Experiments were carried out on the ability of single legs of the whole ghost crab Ocypode ceratophthalma to learn to avoid the receipt of electric shocks coupled with leg position (the Horridge paradigm). Ocypode is a common, hardy, very active, air-breathing subtropical species. Aversive shocks were delivered through a silver wire attached to the dactylopodite whenever the leg was lowered into a dish of sea water. Tests were made comparing position (P) animals with yoked (random, R) controls, on intact crabs and also ones from which the cerebral ganglion had been removed. Preparations that showed leg-position learning were then subjected to further training by bringing them sufficiently close to the water to receive shocks again. All of the animals tested showed some initial improvement in shock avoidance. This was always achieved by the use of one or more natural flexion movements, the commonest being at the meropodite/carpodite, followed by the coxopodite/basipodite, and the propodite/dactylopodite. In successive training, progressively greater flexion was achieved by the use of one or more additional joints. Debrained animals learned better than intact ones. Yoked controls performed badly and often did not learn at all when tested as position animals immediately after the animal they were linked with had learned to avoid shocks. Learning occurred about six times as fast as in comparable insect preparations, under 2 min compared with an average of 8 min. But retention, either with or without reinforcement, was much shorter in the crab preparations than in their insect counterparts; 3 to 4 hr compared with 2 days or more. It is concluded that crab preparations may be valuable for exploration of the cellular neuronal mechanisms underlying shock-avoidance leg-position learning.

Mechanism of Supercontraction in a Striated Muscle Fiber

Cross-striated muscle fibers may contract reversibly to less than 30 percent of their rest length and it is not easy to reconcile this fact with the sliding filament model of muscular contraction. The mechanism of supercontraction has been studied in fibrils obtained from the giant muscle fibers of the barnacle Balanus nubilus. They were examined by phase-contrast light microscopy and electron microscopy. Contraction beyond the 50-percent stage was found to be achieved largely by the passage of thick filaments through the Z-disks, which are perforated. The overlap of thick filaments from adjacent sarcomeres causes the appearance of the contraction bands about the Z-disks. Subsequent contraction is associated with a folding and loose coiling, but not a shortening, of the thick filaments.