Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well

Abstract

Equipped with a mini brain smaller than one cubic millimeter and containing only 950,000 neurons, honeybees could be indeed considered as having rather limited cognitive abilities. However, bees display a rich and interesting behavioral repertoire, in which learning and memory play a fundamental role in the framework of foraging activities. We focus on the question of whether adaptive behavior in honeybees exceeds simple forms of learning and whether the neural mechanisms of complex learning can be unraveled by studying the honeybee brain. Besides elemental forms of learning, in which bees learn specific and univocal links between events in their environment, bees also master different forms of non-elemental learning, including categorization, contextual learning and rule abstraction, both in the visual and in the olfactory domain. Different protocols allow accessing the neural substrates of some of these learning forms and understanding how complex problem solving can be achieved by a relatively simple neural architecture. These results underline the enormous richness of experience-dependent behavior in honeybees, its high flexibility, and the fact that it is possible to formalize and characterize in controlled laboratory protocols basic and higher-order cognitive processing using an insect as a model.

Context-dependent olfactory learning monitored by activities of salivary neurons in cockroaches

“…In a recent study, we have suggested that association between olfactory CS and sucrose US in elementary olfactory learning of salivation in cockroaches takes place in the calyces or the lobes of the mushroom body (Watanabe, et al, 2011). This is in accordance with reports that the mushroom bodies participate in elemental associating olfactory learning in honey bees (Menzel, 2001) and fruit-flies Drosophila (Berry, Krause, & Davis, 2008;Davis, 2005;Heisenberg, 2003;Waddell, 2010), although contribution of the antennal lobe (the primary olfactory center) has also been demonstrated (in honey bees: Giurfa, 2007;Menzel, 2001;in fruit-flies: Thum, Jenett, Ito, Heisenberg, & Tanimoto, 2007;in moths: Daly, et al, 2004). In cockroaches, the mushroom bodies have been shown to receive visual stimuli, as well as olfactory, gustatory and mechanosensory stimuli (Li & Strausfeld, 1997;1999;Mizunami, Okada, Li, & Strausfeld, 1998;Nishikawa, Nishino, Mizunami, & Yokohari, 1998), and thus the mushroom bodies are candidate site for the configural association for context-dependent olfactory conditioning of salivation.…”

“…Recently, we reported classical conditioning of salivation and associated activity changes of salivary neurons in the restrained cockroach (Watanabe & Mizunami, 2006, 2007Watanabe, Sato, Kuramochi, Nishino, & Mizunami, 2008). Salivation in cockroaches is controlled by two salivary neurons of the subesophageal ganglion and a few neurons of the stomatogastric nervous system, axons of which are contained in the salivary duct nerve (Ali, 1977;Davis, 1985;Rotte, White, Blenau, Baumann, & Watz, 2009;Whitehead, 1971).…”

Conceptual learning by miniature brains

“…Among insects, the honeybee has emerged as a powerful model for the study of associative learning [12,14,15,[19][20][21]. In a natural context, bees learn and memorize the local cues characterizing the places of interest, which are essentially the hive and the food sources [22][23][24][25].…”

Participation of NO signaling in formation of long-term memory in salivary conditioning of the cockroach

“…In honey bees, it has been shown that the antennal lobe (primary olfactory center) and the mushroom body (multisensory association center) participate in olfactory learning [5,14,15] and that some neurons in both brain areas exhibit NOS activities [19]. It has been shown that local uncaging of cGMP (but not NO) in the antennal lobe facilitates LTM formation in honey bees [20].…”