Are specific sometimes minute aspects of a situation that activate fixed action patterns?

Neural Basis of Learned Behavior

Owing to the flexibility of neurobiological mechanisms, the earliest response of animals to changes in environment is behavioral. The new behavior is a learned behavior intended to avoid or neutralize harmful effects of the changed environment and represents not an off-the-shelf solution of the type of the innate behavior.

Despite the striking differences from innate behaviors, learned behaviors as well are products of the activity of neural circuits. For patterning and executing learned behaviors, animals use existing species-specific FAPs by modulating the respective neural circuits. Learned behavior might not be perfectly adaptive under the changed conditions of environment, for acquisition of learned behavior is not an “all-or-none” process. Although learned behaviors may be initially imperfect, they may be beneficial because the survival in a drastically changed environment does not necessarily require a perfect behavioral adaptation from the beginning; once the changed behavior makes the survival possible, perfection of the behavior and adaptive morphophysiological changes may follow.

Acquisition of new behaviors is facilitated by the fact that

First, changes in the environment often are represented by contrasting conditions of living, for example aquatic/terrestrial habitat, moist/dry terrain, cold/warm weather, short/long photoperiod, abundance/scarcity of food, herbivorous/carnivorous diet, or presence/absence of predators, which are not as numerous as their intermediate states would be, and

Second, often the same FAPs can serve more than a single purpose:

Learning involves a single set of basic processes which are shared throughout the animal kingdom from molluscs to man.

Gould (1982, p. 261)

In this sense, the learning and innate behaviors share a common neural basis. As pointed out earlier, lampreys can modulate the same central motor program of a basic undulatory pattern to perform different forms of locomotion such as swimming, burrowing, and crawling. The same CPG is conserved across metazoans, and it would, in principle, allow them to switch from an aquatic to a terrestrial form of locomotion in cases when the habitat changes from aquatic to a telluric one. Further, when an animal changes its behavior, it can do this by switching to new patterns of connections between the same neurons of the circuit as it occurs with neurons that control the lobster’s eating and digestion.

Third, there is experimental evidence showing that neural elements and connections for performing a behavior may be conserved after a species has lost the behavior. This may greatly facilitate the “learning” of the new behavior: activating an ancestral circuit may be all that is required for performing the new behavior.

So, both innate and learned behaviors are based on essentially similar neurobiological mechanisms. We know that even an innate behavior can be modified as a result of feedback action, i.e., of its disadvantageous consequences, and to the contrary, behaviors learned at early stages of life are very little, if at all, modifiable (the phenomenon of behavioral imprinting).

Any learned behavior is generally based on the existence and use of innate motor programs or motor program preadaptations. These programs may exist as “out of service” preadaptations still available for reactivation. Over time, by repeated practicing for varying periods of time, the learned behavior may be stereotyped and performed automatically, similarly to an innate behavior, or to its elementary unit, FAP. If it is indeed the case, we might reasonably assume that the learned behavior is based on formation of a specific neural circuitry. If the learned behavior happened to be a lost ancestral innate behavior, the relevant circuit may be identical or similar to the neural circuitry used by ancestors for performing the innate behavior.

The fact that the learned behavior is based on specific motor programs on which the innate behaviors are based suggests that their neural circuitry, as a system of nerve cells that cooperate in generating and controlling that behavior, may be similar to the circuitry for the innate behavior. Says Gould (1982, p. 177):

The emerging picture of motor behavior, then, whether it be the wholly innate performance of spiders, the goal-directed-learning of infants, or the plastic learning we see in piano playing, is that all are routines stored, either from the outset or ultimately, as discrete neural programs.

and

Beethoven’s continued mastery throughout his encroaching deafness is a triumphant instance of how hardwired a motor program can become. (Gould, 1982, p. 176)

Simple behaviors, based on FAPs, can be learned, and there is no alternative left on how a “complex behavior” could be learned by animals, but by integrating the respective FAPs, i.e., their neural circuits, in interacting neural networks.

The phenomenon of imprinting also demonstrates the common physiological basis and the continuity of innate and learned behaviors. In the Konrad Lorenz’s example, Graylag geese are born with an instinct for adopting as mother something that is bigger than themselves, that is closer to them, and that provides food, rather than a mother-resembling figure. By fulfilling all these criteria on his own, the biologist got the newly hatched geese to follow him as their own mother. He succeeded in diverting the natural course of the innate behavior of the young birds because they inherited an innate behavior to look for their mother, neglecting any sensory cues for recognizing her.

This change in behavior is epigenetic by nature, i.e., it involves no change in genes. Such epigenetic changes in both learned and innate behaviors may be induced not only during postnatal life but also during the embryonic and intrauterine development in placentals and oviparous animals. Maternal glucocorticoids from stressed mothers may transplacentally affect the postnatal phenotype (behavior, morphology, and life history) of the offspring. Experimental administration of corticosterone in eggs of the ovoviviparous lizard Lacerta vivipara leads to altered antipredator behavior (less-risky behavior indicative of increased fear or anxiety) in the corticosterone-manipulated offspring. Investigators believe that early hormone exposure as a result of maternal stress could be an important evolutionary factor generating epigenetic variation in natural populations (Uller and Olsson, 2006).

Experimental increase of the testosterone level in female dark-eyed juncos (a small American sparrow), besides its known consequences in male offspring, increases the responsiveness of the hypothalamic–pituitary–adrenal (HPA) axis and intrasexual aggression but weakens the cell-mediated immune response (Zysling et al., 2006). Injection of the neuropeptide corazonin in locusts L. migratoria induces their transition into the gregarious phase, which implies gregarious behavior (including flying), changes in the morphology, and dark pigmentation. In this context, it is important to remember that production of corazonin in the locust’s nervous system is the result of a manipulative expression of the gene through activation of a circuit of the gene for the neurohormone.

Often, learned behaviors are associated with functional and structural changes in nerve cells and in the CNS. In canaries, for example, singing is related to a part of their forebrain. Three forebrain nuclei are involved in normal singing, nucleus hyperstriatum ventralis, pars centralis (HVc), and nucleus robustus archistriatalis (RA). Two nuclei (HVc and RA) normally are, respectively, 99% and 76% larger in the spring (when birds learn new songs) than in fall (Prosser, 1991). Male canaries are the only sex that learns to sing, and their nucleus hyperstriatum ventralis is larger than that of females. Moreover, males that have a longer repertoire of songs have that part three times larger than others (Alcock, 1989).

In zebra finches, the circuits responsible for vocal learning and singing in the cortical nucleus lMAN undergo striking changes in morphology, in size, and axonal arbors during juvenile male development (Iyengar et al., 1999). Although neural circuits are conserved in the course of metazoan evolution, even small changes in neuronal circuits in various species can produce new species-specific behaviors (Katz and Harris-Warrick, 1999).

1 Courtship Behavior of Drosophila melanogaster

Male courtship behavior of D. melanogaster is composed of fixed action patterns of motor acts (Figure 3.1(A),), and thus is an innate program that can be generated practically without the involvement of learning (Bastock & Manning, 1955; Greenspan & Ferveur, 2000; Hall, 1982). When a male fly finds a female, he orients his body axis toward the female (orientation) and starts to chase her (following) with or without prior touching of the female abdomen with his foreleg (tapping). While chasing the female, the male fly extends and vibrates his wings, one wing at a time, generating patterned sounds called courtship songs, which are composed of two components, a humming sound called the sine song and a series of tone pulses called the pulse song (singing). The male fly then approaches the female from behind and licks her genitalia (licking). The male then attempts to mount her back (attempted copulation) and, when successful, connects his genitalia with hers (copulation). Copulation typically persists for 15–25 min depending on various conditions.

Wild-type females never show courtship behavior of the type described above for males. Instead, females exhibit acceptance or rejection of a courting male (Ferveur, 2010). Initially, a virgin female tends to run away from the courting male, but upon sustained exposure to the courtship song, she slows her locomotion with occasional stops (Connolly & Cook, 1973; Manning, 1967; Nakano et al., 2001). When her receptivity has risen sufficiently high, she allows the male to mount and copulate. A recently fertilized female, when courted by a male, displays rejection actions, including decamping, abdominal curing, leg fending, wing fluttering, and ovipositor extrusion. An immature virgin female of less than ∼2 days after eclosion repels a courting male by showing similar rejection actions except for ovipositor extrusion (Connolly & Cook, 1973; Manning, 1967; Nakano et al., 2001).

fru mutant males exhibit a variety of defects in courtship (Hall, 1977). Males with the fru1 allele, which exhibit altered fru expression in the central nervous system (CNS) (Goodwin et al., 2000; Lee & Hall, 2001), court both males and females, while the wild-type males show persistent courtship only toward a female (Gill, 1963; Hall, 1977). fru1 males, however, do not copulate (Gill, 1963). fru alleles devoid of fru expression in the CNS (Lee & Hall, 2001) show extremely reduced courtship activities, which are directed more to a male than to a female (Villella et al., 1997). When fru mutant males are grouped together, they occasionally court each other, forming a chain of courters (Hall, 1977). The courtship song generated by fru mutant males is aberrant, i.e., the interval of individual pulses in the pulse song is longer than normal and the tone pulse is polycyclic, in contrast to the wild-type pulse, which is monocyclic (Villella et al., 1997). fru1 males often exhibit bilateral wing display, extending and vibrating both wings at one time, and this behavior is rarely seen in courtship by wild-type males (Hall, 1977). Despite the striking changes in male courtship, loss-of-function fru mutant females appear to retain normal mating behavior (Villella et al., 1997). These observations suggest that fru plays a central role in generating courtship behavior in wild-type males but not wild-type females.

2.2 Behavioral Modules

Lorenz considered behavior to be composed of basic modules: e.g., classical reflexes, species specific Instinktbewegung ‘Fixed Action Pattern’ (FAP), in later years Erbkoordination, erbkoordinierte Bewegung (1978) (in English: ‘fixed motor pattern’), specific circuits for the environmental control of reflexes and FAPs: ‘Innate Releasing Mechanisms’ (IRM, angeborener Auslösemechanismus), ‘appetites and aversions’ (Stimmungen), etc. Such modules provide each organism with basic behavioral skills to navigate within its environment, detect necessary resources, avoid danger, and interact with conspecifics. Learning can enter in various ways at the level of each of these modules, e.g., in the case of a reflex as ‘conditioned reflex.’

This FAP/IRM diad is basically an extension of the classical Stimulus/Response concept, enhanced by several new features: the classical reflex, activated only by a specific external stimulus, cannot account for the observation that ‘a healthy animal is up and doing’ (as W. McDougall so aptly remarked). Consequently, the spontaneous nature of behavior, in general, and especially in many typical FAPs (locomotion, courtship behavior, certain types of bird song, etc.) became a topic of special interest (FActionP). FAPs constitute much more complex patterns than any of the classical reflexes (FAPatterns) and particular spatiotemporal parameters of FAPs are highly stereotyped within any one species (FixedAP), but different between species. Lorenz exemplified the complex interaction between internal and external variables in his ‘psychohydraulic’ model (1950a, 1978), and applied this reasoning to explain the control of aggression in animals and humans (1963).

It was basically for this work on behavior modules, which are central to ethology, that Lorenz, Niko Tinbergen, and Karl von Frisch shared the distinction of winning the 1973 Nobel Prize for Medicine ‘for their discoveries concerning the organization and elicitation of individual and social behavior patterns.’

E Development of the capacity for intrinsic motivation

The beauty of the IM system is that it too can develop to adapt to enormously diverse environments. In contrast to species with fixed action patterns that dictate its members’ responses to specific types of situations, IM in humans is designed to allow our big brains the opportunity to sculpt this “seeking system” to highly varied activities, subject matter, and goals. Just as developmental experiences help shape other psychological systems (i.e., to improve our working models of attachment and refine our emotional sensibilities), they can help us develop knowledge and skills that allow us to experience IM in highly varied task situations and within different culture contexts. We must view IM as an “epigenetic system” (Rutter, Moffitt, & Caspi, 2006), which allows humans to develop motivated engagement in diverse domains of expertise.

What develops in the development of IM includes competencies at multiple levels. The research we reviewed suggests that people can build domain specific skills that allow them to engage in an activity at higher degrees of challenge and complexity (Csikszentmihalyi, 1990). They can develop individual dispositional interests—enduring knowledge, skills, and emotional associations that support deeper, more stable engagement in an activity (Hidi & Renninger, 2006). They can also develop values, meanings, and personal or collective connections to an activity, which become integrated into the self and make the activity more congruent with one's goals and identity (Ryan & Deci, 2000). Development, then, can be a major determinant of IM.

Further, as young people move into adolescence, they have increased potential to control this development: to deliberately develop skills for regulation of the factors that shape IM (Lerner, 2002). As we said at the chapter outset, teens gain the potential to acquire meta-cognitive understanding and executive skills for controlling their psychological processes (Kuhn, 2009; Steinberg et al., 2006). But there is no guarantee a given youth will gain this control. Ordinary experience may not provide much impetus for developing these advanced levels of thinking. Klaczynski (2004) argues that in daily life, people do most of their thinking using expedient mental shortcuts and heuristics.

What is especially important about IM is that (as reviewed in Section II) it is a state in which adolescents are likely to activate these meta-cognitive and executive skills. They are more likely to process information at deeper levels: asking questions, processing meaning, engaging in more expansive, and integrative reasoning. We suggest then that IM is a state in which this deeper thinking is likely to include analysis and synthesis that helps them understand the determinants of their motivation and develop skills for regulating it.

Research suggests that this happens for many youth. Renninger (2010) observed that high-school students with well-developed interests were able to weigh and choose between competing goals, identify obstacles, and regulate their work to sustain engagement in their domain of interest. We suspect that adolescents are capable of learning to read the emotional cues of boredom and anxiety to adjust a task to keep themselves in a channel of IM. We also propose that adolescents have the potential to learn general skills for self-regulation of motivation that—with effort—can be transferred from one activity to another.

Of course, just because there is “potential” for these differing components of IM to develop in adolescence, it does not mean that they will. They can fail to develop or start to develop and be “snuffed out”. This turns us to the urgency of our next topic.

The Ethological Method

Classical ethology, as exemplified by the work of Lorenz (1965, 1981), maintained that most behaviors important for adaptation to an environment are innately determined fixed action patterns, each performed in a stereotyped way whenever it is released by a specific configuration of stimuli. The theoretical content of Lorenzian ethology has been criticized by Lehrman (1970) and many others. Nevertheless, the emphasis on patterns of behavior expressed by freely moving animals has much to recommend it. The modern ethological approach (Lehner, 1996) emphasizes methods for observing behavior, while eschewing the genetic determinist ideology of Lorenz (Gerlai, 1999; Martin & Bateson, 2007). Ethologists conduct experiments that alter stimulus conditions to analyze causes of behavior patterns (ten Cate, 2009), but they strive to make the stimuli very similar to what the species would encounter in the wild.

The ethological method stresses the importance of watching the animal and identifying distinct postures or patterns of movements exhibited in certain situations. The ethogram is the collection of all distinct behaviors expressed by a mouse (Schellinck, Cyr, & Brown, 2010). Eisenberg (1968) identified 78 behaviors. Each is given a unique name, as shown in Table 10.1, for an abbreviated list of more than 60 distinct behaviors. The typical duration of a distinct behavior is short, ranging from about one second for a tail rattle, to several seconds for chewing while holding a piece of food. For almost all of these, it is essential that a well-trained human observer score the stream of behavior. Mice can move quickly from one behavior to another, and the scoring may be facilitated by a video recording that can repeat the action at a slower speed (Branchi, Santucci, Puopolo, & Alleva, 2004). To a human, a mouse fight may appear to be a blur of paws, tails, and fur with bedding material flying around the cage to complicate things even more. In slow motion, however, the bout appears to be an elaborate sequence of thrusts, kicks, and sometimes bites. Usually one mouse is the initiator of a bout of agonistic behavior and the other defends itself, but these roles can change dynamically during the course of a fight. A good ethological record gives the sequence of each kind of behavior, rather than just stating that there was a mouse fight or that two mice were mating. Later, during the analysis phase of the study, it may be convenient and helpful to aggregate fine-scale behaviors into molar categories.

Table 10.1. Categories of Behaviors in the Ethogram of the Mouse

An epoch of behavior can be scored by tallying the number of occurrences of each distinct pattern. In principle it is also possible to determine the duration of each behavior, but in practice this is very difficult and almost certainly requires slow motion video playback. When examined in microscopic detail, the transition between one behavior and another may not always provide a convenient cue that one has stopped and the next has begun.

If the test situation is relatively simple and there is only one mouse to be scored for a short time, continuous sampling can be employed; a key on a computer or handheld device is depressed every time a different behavior begins. For more complex situations with more than one animal, the demands of continuous sampling on the observer become onerous. Time sampling in which behavior is scored on cue every few seconds is better suited for longer and more complex streams of behavior. It yields a relative frequency count of different behaviors, estimates the duration of particular kinds of activities, and documents transitions from one kind of behavior to another. Software such as Observer XT from Noldus Information Technology is useful for recording distinct behaviors with a time stamp for later analysis, and it functions well for both continuous and time sampling methods.

Several computerized video-tracking systems purport to distinguish distinct behaviors in a simple environment such as an open field (see Chapter 14), while careful placement of photocells may detect specific actions in some kinds of apparatus, such as a head dip on an elevated plus maze. Any attempt at automating the ethogram must be rigorously validated against the opinion of skilled observers.

It is best practice to label behaviors according to the topography of the action, rather than imputing a purpose or function to a sequence of actions. Purpose is an inference from facts, whereas data should consist of facts. If a mouse urinates in a novel environment, the act of urination is observable. Whether this may also qualify as territorial marking cannot be determined from the mere fact. Several other kinds of behaviors impute motive or goal: foraging, hoarding, burrowing, aggression, and reproduction. Each of these can be better recorded in terms of distinct behavior patterns that may or may not culminate in some end result. For example, digging may result in a burrow, but the mere act of digging is not proof that the animal is trying to construct a burrow. Likewise, reproduction is sometimes the consequence of mating behavior, but it is unlikely that the cavorting mice have a well-formed idea of what is going to happen 19 days later. On a descriptive level, mice engage in sexual behavior, not reproduction.

Anyone who watches the antics of a mouse or a pair of mice for only a few minutes in different situations will note how the range of behaviors expressed depends strongly on the situation. This is obvious for things that occur only in a social context, such as mating and agonistic interactions; isolated individuals do not perform social behaviors. Likewise, digging behavior will be seen only when there is a medium in which to dig. When several mice are released into a large and complex environment, as was done in McClearn‘s hypothesis generation apparatus at the Institute for Behavioral Genetics (Chapter 1), almost the complete range of all mouse behaviors may be apparent over a period of several hours or days. This is an excellent means to become familiar with mouse behaviors.

For many kinds of behavioral tests, automated measurement of the stream of behavior should be supplemented with ethological observation of postures and patterns that may have special importance in a test situation. In the simple open field, distance traveled, rearing while far from a wall, or leaning against a wall can be transduced effectively with photocell beams. Patterns such as grooming or the “stretch-attend” will not be revealed in the sequence of beam breaks, however. It also is impossible to tell from photocell beam breaks whether a mouse is truly “freezing” or just sniffing intensively at a drop of urine or other interesting object.

When using the ethological method to score sequences of behaviors, the test usually is not standardized and given some special name. If the researcher is interested in courtship and reproduction, it is usually sufficient to place an adult male and adult female into a cage and then watch the action. Placing two males in the same kind of cage can lead to agonistic interactions, whereas housing several females together may result in barbering. It is very important to use the same situation on every test occasion: the same size of box, the same kind of bedding and food, and the same trial duration. The test parameters should then be described in detail in the methods section of a report.

1.10.2.2 Neurobiological Dissociations

The distinction between habitual and goal-directed behavior can also be made at the level of neural circuitry. Vertebrates and invertebrates both show parallel circuitry for reflexive behavior – including unconditional reflexes and species-typical fixed-action patterns on the one hand, and conditioned reflexes on the other – and voluntary behavior. For example, there are two circuits that mediate tail-flick escape behavior in the crayfish (Procambarus clarkii): one that mediates rapid and automatic escape responses and one that mediates slower and more flexibly controlled responses (Wine and Krasne, 1972; Edwards et al., 1999; see Figure 9).

The rapid escape reflex in response to abrupt stimulation, such as a sharp tap to the side of the abdomen, is a fixed-action pattern that is mediated by medial giant (MG) command neurons. Intracellular recordings from the MGs detect electrical responses in as little as 10 ms after the tap stimulus is applied. The nongiant system, which is excited by gentle prodding and pinching, mediates longer-latency responses that are under a much greater degree of control by the animal than are the immediate escape behaviors. The nongiant neural circuitry innervates and controls the same muscle systems as do the MGs, but it is much more complex (Figure 9) in both the interconnections and the number of layers between the sensory and motor neurons. Although much less is known about the functional control by the nongiant system, presumably it allows for a finer degree of control over the timing and direction of the movement and may even monitor actions as they are planned to allow for corrective feedback prior to execution of the action (see Section 1.10.4.1).

The distinction between the neural basis of the habit system and the voluntary or goal-directed action system can be made in vertebrates as well. There is not sufficient space here to adequately review the extensive literature on this dissociation, but it appears that, in mammals at least, S-R habit learning can be mediated at many locations within the nervous system, including the spinal cord (Chen and Wolpaw, 1995), the basal ganglia (White, 1989), and the striatum (Yin et al., 2004), whereas goal-directed R-O learning is mediated by cortical structures, such as the prelimbic area and the insular cortex (Balleine and Dickinson, 1998a).

1.06.3.2 Neurobiological Dissociations

The distinction between habitual and goal-directed behavior can also be made at the level of neural circuitry. Vertebrates and invertebrates both show parallel circuitry for reflexive behavior—including unconditional reflexes and species-typical fixed-action patterns on the one hand, and conditioned reflexes on the other—and voluntary behavior. For example, there are two circuits that mediate tail-flick escape behavior in the crayfish (Procambarus clarkii), one that mediates rapid and automatic escape responses and one that mediates slower and more flexibly controlled responses (Edwards et al., 1999; Wine and Krasne, 1972; see Fig. 10).

The rapid escape reflex in response to abrupt stimulation, such as a sharp tap to the side of the abdomen, is a fixed-action pattern that is mediated by medial giant (MG) command neurons. Intracellular recordings from the MGs detect electrical responses in as little as 10 ms after the tap stimulus is applied. The nongiant system, which is excited by gentle prodding and pinching, mediates longer-latency responses that are under a much greater degree of control by the animal than are the immediate escape behaviors. The nongiant neural circuitry innervates and controls the same muscle systems as do the MGs, but is much more complex (Fig. 10) in both the interconnections and the number of layers between the sensory and motor neurons. Although much less is known about the functional control by the nongiant system, presumably it allows for a finer degree of control over the timing and direction of the movement and may even monitor actions as they are planned to allow for corrective feedback prior to execution of the action (see section Making Things Happen).

The distinction between the neural basis of the habit system and the voluntary or goal-directed action system can be made in vertebrates as well. There is not sufficient space here to adequately review the extensive literature on this dissociation, but it appears that in mammals at least S–R habit learning can be mediated at many locations within the nervous system, including the spinal cord (Chen and Wolpaw, 1995), the basal ganglia (White, 1989), and the striatum (Yin et al., 2004), while goal-directed R–O learning is mediated by cortical structures, such as the prelimbic area and the insular cortex (Balleine and Dickinson, 1998a). Similar pathways and circuits appear to be involved in modulating these two forms of instrumental control (Balleine and O'Doherty, 2010).

Female Behavior

In many Drosophila species, females do not perform the complex series of display behaviors seen males. Instead, their role is to elicit courtship from males through the production of aphrodisiac pheromones. These chemicals stimulate Drosophila males, acting as the sign stimuli that trigger the fixed-action pattern of male courtship behavior. In Drosophila melanogaster, mature females produce a 27-carbon aphrodisiac pheromone whose chemical name is (Z,Z)-7, 11-heptacosadiene. This compound, when applied to a small wad of cotton, can elicit courtship from males. However, visual cues are also important for normal sexual behavior. So, while blind mutant males can court, and wildtype males can court in the dark, these situations do not produce typical sexual behavior. Males in these circumstances have difficult time tracking the females when they run away.

For the most part, in a species like Drosophila melanogaster, females initially move away from a courting male. In fact, the majority of female sexual behaviors are related to their initial unwillingness to mate. Unreceptive females kick at courting males, and flick their wings at them. However, once pursued, the male’s song appears to cause the female to slow down and stop performing rejection behaviors. Eventually a courted female stops altogether and, when receptive, opens vaginal plates to allow the male to mate with her. It appears that in terms of copulation, females are completely in control.

In many Drosophila species, copulation causes dramatic changes in the biology of the female. These changes are caused by chemicals provided by the male during copulation. In D. melanogaster the major effects are caused by a chemical known as sex peptide, which the male delivers to the female prior to delivering sperm. Within hours of copulation the effects of this chemical can be detected in the “mated female.” She stops production of the aphrodisiac pheromone, causing her to be less attractive to other males. She also undergoes changes that make her less likely to be sexually receptive if a male does court her. These effects result in the female becoming an essentially non-sexual organism and last (again, in D. melanogaster) for about 5 days (see Chapman et al. (2003)).

The evolution of compounds like sex peptide, delivered by males, to females, during copulation, are likely a result of a phenomenon known as sperm competition. Since courtship is such a costly process for the males, in terms of time and energy, it is crucial that a male protect his investment in the next generation. If a recently-mated female was to copulate with another male, she might use his sperm preferentially over the sperm of the male who originally mated with her. Therefore, a system has evolved in males to provide chemicals that reduce the chances that the females with whom they mate will re-mate again quickly. The effects of compounds, like sex peptide, act for a period of days, during which the female lays eggs fertilized by the male that provided the sex peptide along with his sperm. She may lay hundreds of eggs before the effects of sex peptide wear off. She then becomes sexually attractive, and sexually receptive, again. The negative to this entire process is that sex peptide has been shown to shorten the life of females. Thus, we may someday see the evolution of systems within the female to counteract the effects of sex peptide.

Automatic Response

As described above, the handful of empirical studies on ticklish laughter suggest that it is not a response driven by positive affect nor does it require an interpersonal context. So what does underlie gargalesis?

The data that exist seem most amenable to the view that gargalesis is a relatively automatic, low-level physiological response. This general view is consistent with the writing of G. Stanley Hall and Francis Bacon and has been advocated by several researchers in more recent times. Findings to date have not revealed exactly what mechanism controls the response but likely candidates are that it is a type of complex reflex or fixed action pattern. In literature on human behavior, the term, fixed action pattern, is sometimes replaced with terms such as species-characteristic or species-typical stereotyped motor pattern requiring a particular releasing stimulus. The boundaries between reflexes and other species-typical behavioral dispositions remain controversial. Reflexes are distinguished from fixed action patterns based on their graded character: the more intense the stimulation the more intense the response. It currently is not known whether ticklish laughter shows an all-or-none character like a fixed action pattern or a graded response to the magnitude of stimulation as with the typical reflex.

If gargalesis is some type of complex reflex or species-typical stereotyped behavior, then why can we not elicit it in ourselves? After all, we can tap our own knees and produce the knee-jerk reflex. There are, however, other reflexes that one cannot elicit in oneself – startle being a prime example. Startle and tickle appear to share some features. Both appear to require some element of unpredictability or surprise – one can no more tickle oneself than startle oneself (at least, not without the use of some external device such as a gun). The two states also produce facial expressions that resemble the types of expressions elicited during emotion, but are arguably not emotional states in and of themselves. The proposition that tickle is a reflex, or other kind of innate stereotyped motor pattern, does not imply that the tickle response is unmodifiable or unaffected by mood or other psychological states. For example, the startle reflex can be potentiated by negative emotion while the opposite effect is produced by positive emotional states and even by a faint warning signal. Despite the name, ‘fixed action patterns’ also permit substantial variability in behavior.

There is also another explanation consistent with gargalesis being a low-level physiological process and with one not being able to produce it in oneself. Lawrence Weiskrantz and his colleagues, in a paper that appeared in Nature in the 1970s, suggested that the neurological processes observed in vision might provide an answer. When the eyes dart from one focal point to another, the world does not appear to jump because the brain takes into account that it has issued a command (efferent signal) to move the eyes. Weiskrantz and colleagues reasoned that similarly when the brain issues the command to self-tickle, it sends a message to cancel the sensation of ticklishness. Thus, what is sometimes termed exafference (stimulation uncorrelated with a motor command) may be required to elicit the tickle response.

Fixed Action Patterns and Central Pattern Generators: A Neuroethologic Approach to Behavior

Ethology is the study of whole patterns of animal behavior under natural conditions in a manner that highlights the functions and the evolutionary process of those patterns. With an ever-increasing physiologic approach through the application of refined and elegant laboratory research techniques to animal behavior, neurobiology and ethology have coalesced to develop neuroethology.40

An important behavior type in ethology is the fixed action pattern (FAP). This is an instinctive indivisible behavioral sequence that when initiated will run to full completion. FAPs are invariant and are produced by a neural network known as the innate releasing mechanism in response to an external stimulus known as a sign stimulus.

FAPs are ubiquitous in the animal kingdom and are seen from invertebrates to higher primates. Movements resulting in FAPs may be initiated by central pattern generators (CPGs): “Movements are generated by dedicated network of nerve cells that contain the information that is necessary to activate the different motor neurons in the appropriate sequence and intensity to generate motor patterns. Such networks are referred to as Central Pattern Generators.”41

Tassinari and coworkers recognized that motor events related to certain epileptic seizures and parasomnias share very similar features. This suggests a stereotyped inborn FAP, perhaps initiated by CPGs.42 Tassinari recognized CPGs as genetically determined neuronal aggregates in the mesencephalon, pons, and spinal cord that, from an evolutionary perspective, were linked with innate primal behavior essential for survival (e.g., feeding, locomotion, reproduction).

In higher primates, CPGs are inhibited by the influence of neocortical control. Many of the CPGs are located in the brainstem and in close proximity to processes that govern the wake, NREM sleep, and REM sleep transitions. Despite diurnal neocortical inhibition, Tassinari provides a neuroethologic model whereby both epilepsy and sleep can lead to a temporary loss of control of the neomammalian cortex that is provided a pathway through a common arousal platform initiated by CPGs, which in turn triggers these FAPs (Figure 65-2), resulting in the abrupt onset of bizarre motor or emotional expressions that are uncharacteristic of awake neocortical-mediated diurnal behavior.

Tassinari's concept of the role of CPGs and FAPs provides a physiologic explanation for parasomnias. This concept is particularly useful in sleep forensics because parasomnias and epileptic seizures tend to have patterned stereotyped actions without conscious awareness. When addressing criminal allegations and their potential association with sleep-related conditions, the sleep medicine specialist can use behavior pattern recognition, applying neuroethologic concepts that indicate process fractionation, and neurobehavioral investigative techniques. Such an approach could be particularly beneficial and would be consistent with the direction of current mainstream neuroscience.