Dimensions of Cognition in an Insect, the Honeybee

Dimensions of Cognition in an Insect, the Honeybee Randolf Menzel Freie Universität Berlin Martin Giurfa Université–CNRS Paul Sabatier Emery, & Dickinson, 2003; Emery, 2006; Güntürkün, This review provides evidence for the enormous richness of 2005; Katz, 1950a). Thus, expectation, attention, planning, insect behavior, its high flexibility, and the cross-talk between and decision making could be useful terms for animals, different behavioral routines. The memory structure established even if we assume that they possess only implicit knowl- by multiple forms of learning represents sensory inputs and edge. If such terms are used, we assume that the animal relates behaviors in such a way that representations of complex retrieves a memory whose structure allows two or more environmental conditions are formed. Navigation and com- alternative outcomes to be evaluated and compared munication in social hymenoptera are particularly telling before any motor action is performed. In this article, we examples in this respect, but it is fair to conclude that similar will address the question as to whether it is reasonable to integrated forms of dealing with the environment will be found assume such forms of internal processing in an insect, in other insects when they are studied more closely. In this the honeybee. Specifically, we will ask whether these ani- sense, research addressing behavioral complexity and its under- mals can recollect the contents of their memory without lying neural substrates is necessary to characterize the real expression of sensory-motor routines and use them for potential of insect learning and memory. Usually, such an internal operations and decision making. There are approach has been used to characterize behavioral simplicity good reasons for rejecting this kind of questioning when rather than complexity. It seems therefore timely to focus on the it comes to understanding invertebrate behavior. On the latter by studying problem solving alongside and in addition to other hand, searching for experimental conditions that elemental forms of learning. would allow us to address the internal processing of the brain devoid of sensory-motor control, its spontaneity, Key Words: learning and memory in the honeybee, nav- and its creativity, even in such tiny brains as those of igation, comparative cognition, nonelemental forms insects, may help to do better justice to the complexity of of learning neural functions in bigger brains. WHY USE BEES FOR STUDIES One of the most important distinctions in conceptu- ON COGNITIVE COMPLEXITY? alizing cognition is that between implicit and explicit knowledge. Explicit knowledge may, in a strict sense, Three main reasons justify the use of the honeybee as exist only in humans. Animals might possess only implicit a model for studies on cognitive complexity: (a) behav- knowledge, but this does not exclude the possibility that ioral richness, including complex learning and memory certain forms of knowledge might reach an explicit-like faculties; (b) experimental access in terms of controlled status specific for the animal species in question in the training and testing; and (c) accessibility of the central sense that internal operations on memories are per- nervous system. With respect to the first characteristic, formed without motor expression of such operations. A bees exhibit developed learning and memory capabilities telling example of this form of knowledge is the choice Behavioral and Cognitive Neuroscience Reviews behavior of food-storing birds, which make their choices Volume 5 Number 1, March 2006 24-40 depending on which kind of food they have stored and DOI: 10.1177/1534582306289522 when and where they have stored it (Clayton, Bussey, © 2006 Sage Publications 24 Downloaded from bcn.sagepub.com at UNIV CALIFORNIA IRVINE on October 5, 2016 Menzel, Giurfa / DIMENSIONS OF COGNITION IN AN INSECT 25 that apply to local cues characterizing the places of inter- which has been described as the honeybee dance est, which are essentially the hive and the food sources. At (von Frisch, 1967) because of its use of ritualized, com- these places, honeybees learn, memorize, and discrimi- municative behavior indicating distance and direction to nate colors, shapes, patterns, odors, and textures, among a profitable food source, can be “read” by the experi- other characterstics (Menzel, 1985, 2001). These capaci- menter, who can record dances in one-frame observation ties allow enhanced foraging efficiency and, coupled with hives with glass walls. Dances therefore constitute true learning abilities for landmark constellations and for reports on what the outgoing forager perceived, what it celestial cues (azimuthal position of the sun, polarized learned, and what it considers worth reporting. This light pattern of the blue sky), ensure efficient navigation unique situation was ingeniously exploited by Karl von in a complex environment. The second characteristic is Frisch (1967), who discovered through it a vast range of what makes honeybees useful for the experimenter: They sensory- and experience-dependent capacities. are accessible for controlled training and testing. The work on honeybees has more recently gained Different paradigms have been used to this end, two of from cognitive perspectives (Cheng & Wignall, 2006; which deserve special attention: (a) the olfactory condi- Giurfa, 2003; Menzel, Giurfa, Gerber, & Hellstern, tioning of the proboscis extension response (PER) in har- 2001). Besides the battery of more traditional assays nessed bees and (b) the training of the approach flight allowing the study of behavior mentioned above, new toward a visual target in free-flying bees. In the former, paradigms have been conceived both for studies on free- harnessed bees are trained to associate an odor with a flying bees conditioned mostly with visual stimuli and for sucrose reward delivered to their antennae, which elicits studies on olfactory learning with restrained bees. We the PER (Bitterman, Menzel, Fietz, & Schäfer, 1983; will focus on three main topics that allow appreciating to Takeda, 1961), and then to the proboscis; the association which extent cognitive thinking has impregnated new formed is of Pavlovian nature and enables the odor to studies on bee learning and memory and how this think- release the PER in a subsequent test. In the latter, free- ing has changed our vision of the complexity of this flying individually marked bees are pretrained to fly insect’s behavior. We will concentrate on learning and toward the training/test place and are rewarded with memory as applied in navigation, communication, and sucrose solution whenever they choose the appropriate discrimination. For the first context, studies on naviga- visual target at that place (von Frisch, 1967). In this way, tion between the nest and a goal (a profitable food bees can be trained to visual stimuli such as colors, shapes, source) have in recent years overtaken the traditional patterns, depth and motion contrast, among others. The conceptual framework, which posited that navigation associations built in this context link visual stimuli and along well-defined routes is the main strategy bees use. reward but also the animal’s response (e.g., landing) and The structure of spatial memory in bees was reconsid- the reward, thus representing an instrumental form of ered by adopting a cognitive approach and applying learning. Finally, the third characteristic that makes bees novel forms of experimentation. For the latter case, interesting for cognitive complexity studies is the fact that questions are emerging about the nature of the memo- the neural bases of such complexity can be accessed ries that honeybee dances may activate in dance follow- because of the relative simplicity of the bee nervous sys- ers. This questioning contrasts with the traditional view tem (Menzel, 2001; Giurfa, 2003). PER conditioning has of bees “blindly” following instructions from dance the advantage that it can be combined with a physiologi- behavior with the notion that their own memories about cal approach, allowing the study of the bee brain while the environment may be reactivated by dances that the bee learns or recalls memorized information in vivo. would, in turn, allow combining instructions concerning As the bee is immobilized in such a preparation, it is pos- a goal with known routes toward it. Finally, discrimina- sible to expose its brain through a small window cut in the tion learning in bees also required a change of frame- cuticle of the head. Physiological correlates of the differ- work as the accent is shifted from the study of sensory ent forms of olfactory conditioning can be found at capacities to the question as to how these capacities are different levels, ranging from the molecular and pharma- implemented to solve nonelemental discriminations. cological ones to single identified neurons and neuronal ensembles whose activity can be monitored using modern LEARNING IN A NAVIGATION CONTEXT optophysiological recording techniques. In most behavioral studies, inference about internal Navigation is an orientation strategy that allows ani- processing can be made only indirectly by observing mals to travel between defined locations without having changes in the behavior in question. In the honeybee, direct sensory access to these locations. In this sense, nav- one can additionally study a communicative process igation differs from general orientation and guidance, between foraging animals, transcending the usual limita- which

Load more