CHAPTER 3 Cognitive Components of Insect Behavior Martin Giurfa*,† and Randolf Menzel‡ *Universite´ de Toulouse, Centre de Recherches sur la Cognition Animale, Toulouse, France †Centre National de la Recherche Scientifique, Centre de Recherches sur la Cognition Animale, Toulouse, France ‡Freie Universita¨t Berlin, Berlin, Germany INTRODUCTION foraging,6,7 and they learn the spatial relations of envi- À ronmental objects during these exploratory flights.8 10 Cognition is the integrating process that utilizes Fruit flies (Drosophila melanogaster) also respond to their many different forms of memory (innate and acquired), placement within a novel open-field arena with a high À creates internal representations of the experienced level of initial activity,11 13 followed by a reduced world, and provides a reference for expecting the future stable level of spontaneous activity. This initial elevated of the animal’s own actions.1,2 It thus allows the animal component corresponds to an active exploration because to decide between different options in reference to the it is independent of handling prior to placement within expected outcome of its potential actions. All these pro- the arena, and it is proportional to the size of the arena.14 cesses occur as intrinsic operations of the nervous sys- Furthermore, visually impaired flies are significantly tem, and they provide an implicit form of knowledge impaired in the attenuation of initial activity, thus for controlling behavior. None of these processes need suggesting that visual information is required for the to—and certainly will not—become explicit within the rapid decay from elevated initial activity to spontaneous nervous systems of many animal species (particularly activity within the novel open-field arena.14 invertebrates and lower vertebrates), but their existence Exploratory behavior facilitates learning by associat- must be assumed given the animal’s specific behavioral ing the animal’s action to the resulting outcome. For output. Here, we focus on cognitive components of example, a hungry animal searching for food in a par- insect behavior and analyze behavioral outputs that ticular sensory environment learns upon a successful refer to several forms of internal processing. In doing search the relationship between its own actions, the so, we aim to relate the complexity of the insect nervous external conditions signaling the outcome, and the val- system to the level of internal processing, which is a uating signal of the food reward. This kind of associa- major goal of comparative animal cognition. tion constitutes the basis of operant (instrumental) learning.15 Operant learning has been intensively studied in insects. A classic protocol for the study of this learning form is the flight simulator in which a ACTING UPON THE ENVIRONMENT: Drosophila is suspended from the thorax in the middle EXPLORATION, INSTRUMENTAL of a cylindrical arena that allows the presentation of LEARNING, AND OBSERVATIONAL visual landmarks (Figure 3.1). The tethered fly flies sta- LEARNING tionary and if some of these landmarks are paired with the aversive reinforcement of an unpleasant heat beam Insects, like all animals, explore the environment pointed on the thorax, the fly learns to fly toward a and by doing so acquire relevant sensory, motor, and safe direction, avoiding the dangerous-landmark direc- integrative information that facilitates learning about tions (Figure 3.1).17,18 The fly learns to control rein- À relevant events in such environments.3 5 Honeybees, for forcement delivery as its flight maneuvers determine instance, explore the environment before they start the switching-off of the heat beam if the appropriate Invertebrate Learning and Memory. DOI: http://dx.doi.org/10.1016/B978-0-12-415823-8.00003-4 14 © 2013 Elsevier B.V. All rights reserved. ACTING UPON THE ENVIRONMENT: EXPLORATION, INSTRUMENTAL LEARNING, AND OBSERVATIONAL LEARNING 15 yaw torque signal laser computer diode light torque source meter color filter light guides diffusor electric motor arena position FIGURE 3.1 The flight simulator used for visual conditioning of a tethered fruit fly.16 (Left) A Drosophila is flying stationary in a cylin- drical arena. The fly’s tendency to perform left or right turns (yaw torque) is measured continuously and fed into a computer, which controls arena rotation. On the screen, four ‘landmarks,’ two T’s and two inverted T’s, are displayed in order to provide a referential frame for flight direction choice. A heat beam focused on the fly’s thorax is used as an aversive reinforcer. The reinforcer is switched on whenever the fly flies toward a prohibitive direction. Therefore, the fly controls reinforcer delivery by means of its flight direction. (Right) Detail of a tethered fly in suspended flight within the simulator. Source: Courtesy of B. Brembs. flight directions are chosen,18 thus constituting a case An important point raised by this example of of operant learning (see Chapters 2 and 28). observational learning is that it would have to take Furthermore, insects are also endowed with the the form of higher order conditioning because the capacity to learn about the actions produced by others, observer cricket would not actually directly experi- be they conspecifics or not.19 Wood crickets (Nemobius ence the unconditional stimulus of a spider attack, sylvestris), for instance, learn to hide under leaves by which would result in immediate death, thus making observing experienced conspecifics in the presence of a learning superfluous. That insects are capable of natural predator, the wolf spider.20 Observer crickets such higher order conditioning, specifically second- were placed in a leaf-filled arena accompanied by con- order conditioning, has been shown in various cases. specifics (demonstrators) that were either confronted Honeybees and fruit flies learn such second-order with a wolf spider and therefore tended to hide under associations. Whereas flies exhibit second-order condi- leaves or did not experience this predatory threat. tioning in an aversive context, in which they learn Observers that interacted with spider-experienced con- to associate an odor (conditioned stimulus 1 (CS1)) specifics were more likely to hide under leaves than with shock (unconditioned stimulus (US)) and then observers that interacted with conspecifics that had a second odor (conditioned stimulus 2 (CS2)) with the no recent spider experience. This difference persisted previously conditioned CS1,21 honeybees learn second- 24 hr after demonstrators were removed from the order associations in an appetitive context while experimental arena, thus showing that perception of searching for food. They learn to connect both two À danger in observers had been altered by the demon- odors (odor 11 sucrose reward; odor 2 1 odor 122 24) strators’ behavior.20 Crickets did not hide under leaves and one odor and one color.25 Although these exam- when separated from demonstrators by a partition that ples refer to the framework of classical (Pavlovian) allowed for pheromone exchange between compart- conditioning in which animals learn to associate ments but not visual or physical contact, nor did they different stimuli,26 similar explanations could be pro- increase their tendency to hide when placed in arenas vided for operant learning situations, thus rendering that had previously contained crickets confronted with the higher order conditioning explanation of observa- spiders. Thus, naive crickets learn from experienced tional learning plausible. demonstrators how to hide under leaves when facing a Observational learning even at a symbolic level is potential threat, and this learning requires a direct con- exemplified by dance communication in bees (discussed tact between observers and demonstrators. later).6 2. CONCEPTS OF INVERTEBRATE COMPARATIVE COGNITION 16 3. COGNITIVE COMPONENTS OF INSECT BEHAVIOR EXPECTATION such shortcuts between a communicated location and a location memorized on the basis of their own experi- Operant learning means that the animal may ence implies that both locations have a common spatial develop an expectation about the outcome of its reference framework. Such memory structure could actions. Two forms of expectation can be distin- store geometric relations of objects in the explored guished: conditioned responding to an experienced environment and could be conceptualized as a cogni- stimulus, as in associative learning, and planning of tive (or mental) map because the behavior of bees meets 8,30 behavior in the absence of the stimuli associated with the definition of a cognitive map. It would include its outcome. Both of these forms of expectation com- meaningful objects at their respective locations and on prising lower and higher cognitive processes interact the way toward them, and thus the animal would know in navigation and waggle dance communication in at any place where it is relative to potential destinations honeybees. Bees navigating toward predictable food allowing to plan routes to locations whose signifying sources follow routes and develop visual memories of signals are not available at the moments decisions are landmarks seen en route and at the locations of food made. sources.8 The locations are qualified in the sense that The term expectation can be applied at multiple the insect expects the formerly experienced target levels of behavioral and neural processes. A low-level signals at specific points of its route. For instance, bees process is the efference copy of the neural