of the three-spined stickleback (Gasterosteus aculeatus), a small fish. Male sticklebacks set up territories in small streams early in the spring, build a nest of bits of plant material, and will generally court any female that may pass through their territory. Courtship includes a zigzag dance by the male, appropriate posturing by the female, leading to and showing of the nest entrance by the male, following and entering the nest by the female, laying eggs, and finally fertilization (see Figure 3.4). The female swims away and the male then courts another female. The male could continue courting egg-laden females for many days, but usually he does not. Experiments in which eggs were removed from or added to the nest have shown that visual stimuli from the eggs inhibit sexual activity: if eggs are removed from the nest, the male will continue courting females, but if eggs are added to the nest he will cease courting, regardless of the number of eggs he has fertilized (Sevenster-Bol 1962). This is an especially interesting example because the same visual stimulus that inhibits sexual activity has an activating effect on the parental behavior (fanning the eggs) of the same male.
Figure 3.4 Courtship and mating behavior of the three-spined stickleback. The male is on the left and the female, with a swollen belly, is on the right. A typical courtship sequence is indicated below the diagram. (From Tinbergen 1951).
Stimuli not only control behavior by their presence, but in many cases continue to affect behavior even after they have physically disappeared. When a stimulus has arousing effects on behavior that outlast its presence, priming is said to occur. Aggressive behavior in the male Siamese fighting fish (Betta splendens) provides a good example (Hogan & Bols 1980). This fish shows vigorous aggressive display and fighting toward other males of its species (including its own mirror image). If a fish is allowed to fight with its mirror image for a few seconds and the mirror is then removed, it is very likely to attack a thermometer introduced into the aquarium. If the thermometer had been introduced before the mirror was presented, the fish very likely would have ignored it. Thus, the sight of a conspecific not only releases aggressive behavior, it must also change the internal state of the fish for some time after the conspecific disappears. We can say that the stimulus primes the mechanism that coordinates aggressive behavior or, more simply, that it primes aggression. Similar priming effects have been demonstrated with food and water in rats and hamsters, and with brain stimulation in several species (see Hogan & Roper 1978). An especially elegant mathematical analysis of priming in cichlid fish and crickets is presented by Heiligenberg (1974).
These examples of priming all occur during the time span of a few minutes. Some stimuli prime behavior over a much longer period. Stimuli from the eggs of the stickleback inhibit sexual behavior, as we have just seen, but they also prime parental behavior. Male sticklebacks fan the eggs in their nest by moving their fins in a characteristic manner, which directs a current of water into the nest and serves to remove debris and provide oxygen to the developing embryos. The amount of fanning increases over the 7 days it takes for the eggs to hatch. It has been shown that CO2, which is produced by the eggs, is one of the stimuli releasing fanning, and the amount of CO2 produced is greater from older eggs. Thus, one might expect that the increased fanning is a direct effect of CO2 concentration. This supposition was tested in an experiment by Van Iersel (1953). He replaced the old eggs on day 4 with newly laid eggs from another nest. There was a slight drop in fanning with the new eggs, but fanning remained much higher than the original day-1 level. Further, the peak of fanning activity was reached the day the original eggs would have hatched. This means that the stimuli from the eggs must prime a coordinating mechanism and that the state of the coordinating mechanism is no longer completely dependent on stimulation from the eggs after 3 or 4 days.
A similar example is provided by the development of ovulation in doves. A female ring dove (Streptopelia risoria) will normally lay an egg if she is paired with an acceptable male for about seven days. If the male is removed after 2 or 3 days, the developing egg regresses and is not laid. However, if the male is allowed to remain with the female for 5 days before he is removed, the majority of females will lay an egg 2 days later. Experiments by Lehrman (1965) and his colleagues demonstrated that it is the stimuli from the courting male that prime the mechanism responsible for ovulation.
Longer-term effects of stimuli can be seen in the yearly cycle of gonad growth and regression in some birds and fish as a result of changes in day length. And changes in day length can also stimulate a host of other physiological changes including those that prepare migratory birds for their long-distance flight (e.g., Piersma & Van Gils 2011) or various mammals for hibernation in the winter (Nelson 2016).
Hormones and other substances
Hormones are substances released by endocrine glands into the bloodstream; many of them are known to have behavioral effects. Lashley (1938) suggested that hormones could affect behavior in at least four different ways: during the development of the nervous system, by effects on peripheral structures through alteration of their sensitivity to stimuli, by effects on specific parts of the central nervous system (central behavior mechanisms), and by nonspecific central effects. Abundant evidence for all these modes of action has accumulated since Lashley’s time, although the mechanisms by which hormones influence behavior have turned out to be more complex and diverse than early investigators realized (Beach 1948).
Both peripheral and central effects of the hormone prolactin are seen, for example, in the parental feeding behavior of the ring dove. Prolactin is responsible for the production of crop “milk” sloughed-off cells from the lining of the crop that are regurgitated to feed young squabs. Lehrman (1955) hypothesized that sensory stimuli from the enlarged crop might induce the parent dove to approach the squab and regurgitate. His experiments showed that local anesthesia of the crop region, which removes the sensory input, reduced the probability that the parents will feed their young. More recent experiments have confirmed that prolactin has both peripheral and central effects on the dove’s parental behavior (Buntin 1996).
The maternal behavior of the rat provides an example that illustrates the variety of hormonal effects. The hormones released at parturition change the dam’s olfactory sensitivity to pup odors, reduce her fear of the pups, and facilitate learning about pup characteristics; they also activate a part of the brain essential for the full expression of maternal behavior (see Fleming & Blass 1994). More extensive coverage of the relation between hormones and behavior can be found in Chapter 6.
Substances released from the neuron terminals into the synapse are known as transmitters; many of these are known to be involved in activating specific behavior systems such as feeding and drinking (see Nelson 2016). Transmitters such as dopamine are thought to mediate the motivational effects of stimuli for a wide range of behavior systems, especially their reinforcing effects (Glimcher 2011). Examples of these effects are given in Chapter 6. Psychoactive drugs, which are thought to exert their effects by altering neurotransmitter functioning in the brain, are also causal factors for behavior, but will not be considered further here.
Intrinsic neural factors
In living organisms, the nervous system is continuously active, and this has many consequences for the occurrence of behavior. Adrian et al. (1931) was the first to demonstrate spontaneous firing of an isolated neuron, and Von Holst (1935) showed that such nervous activity underlay the endogenous patterning of neural impulses responsible for swimming movements in fish. That behavior can occur spontaneously, i.e., without any apparent external cause, was an idea that was long resisted by many behavioral scientists. As we have seen (Chapter 1), there is a long history of behavioral scientists fighting against mentalistic
