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The Olfactory Memory of the Honeybee Apis Mellifera The Journal of Experimental Biology 200, 2045–2055 (1997) 2045 Printed in Great Britain © The Company of Biologists Limited 1997 JEB0825 THE OLFACTORY MEMORY OF THE HONEYBEE APIS MELLIFERA III. BILATERAL SENSORY INPUT IS NECESSARY FOR INDUCTION AND EXPRESSION OF OLFACTORY BLOCKING ROBERT S. THORN AND BRIAN H. SMITH* Department of Entomology, 1735 Neil Avenue, Ohio State University, Columbus, OH 43210, USA Accepted 7 May 1997 Summary The associative learning phenomenon termed ‘blocking’ than the antennae must be crucial for establishing demonstrates that animals do not necessarily associate a blocking. Further experiments show that this bilateral conditioned stimulus (e.g. X) with reinforcement if X is interaction between brain hemispheres is crucial during coincident with a second conditioned stimulus (e.g. A) that both the induction and the expression of blocking. This had already been associated with the same reinforcement. result implies that blocking involves an active inhibition of Blocking therefore represents a tactic that animals can use odor association and recall, and that this inhibition is to modulate associative learning in order to focus on the mediated by a structure that spans both brain hemispheres. most predictive stimuli at the expense of novel ones. Using This interpretation is consistent with a role for identified an olfactory blocking paradigm in the honeybee, we bilateral modulatory neurons in the production of investigated the mechanistic basis for olfactory blocking. blocking. We show that removing input from one antenna eliminates the blocking of one odor by another. Since antennal sensory neurons only project to the ipsilateral antennal lobe in the Key words: memory, honeybee, Apis mellifera, learning, olfactory honeybee, more central processing regions of the brain conditioning, blocking, odor mixtures. Introduction Animals do not always ‘reflexively’ associate a conditioned reinforcement in a way that would produce robust associative stimulus (CS) with an unconditioned stimulus (US). In recent learning if A were not present. Blocking is a widespread years, theoretical accounts of learning have focused on several phenomenon and is central to understanding associative paradigms that demonstrate that animals can regulate whether learning of complex mixtures of stimuli. It was first described a CS enters into an association even though it may be properly by Kamin (1968, 1969) in rat associative conditioning, but has paired with reinforcement (Kamin, 1968, 1969; Rescorla and been found in a variety of other animals, including Wagner, 1972; Macintosh, 1974, 1983; Pearce and Hall, 1980; invertebrates such as honeybees (Smith and Cobey, 1994; Rescorla and Holland, 1982; Rescorla, 1988; Pearce, 1994). Smith, 1996, 1997) and slugs (Sahley et al. 1981), and This flexible association system probably reflects the need to blocking is even found in spinal reflexes (Illich et al. 1994). It extract pertinent sensory stimuli from a confusing, stimulus- may thus represent a basic and widespread tactic for rich environment every time that an animal learns an experience-dependent biasing of sensory processing. association (Smith, 1996). Since animals do not have unlimited Furthermore, blocking is independent of the type of US, sensory capacities, they have evolved strategies for focusing occurring in both appetitive (Kamin, 1968, 1969) and aversive sensory processing capacities on the most useful stimuli. In (Ross, 1985) conditioning, and, at least in the honeybee, it may most instances, this involves tuning sensory systems to stimuli be more robustly expressed among conditioned stimuli from that are predictive, and several central nervous system (CNS) the same sensory modality (Bitterman, 1996). tactics have evolved to facilitate this tuning. Little is known about the neuroanatomical substrates of One such tactic regards a learning phenomenon called blocking. Several studies of vertebrates have found that blocking, in which a CS that has been previously learned (e.g. hippocampal lesions disrupt blocking (Solomon, 1977; Rickett odor A) will substantially overshadow a second CS (e.g. odor et al. 1978), presumably by affecting memory of pretraining. X) that is added to it. The association of X with reinforcement Holland and Gallagher (1993a,b) have produced specific is largely blocked despite the fact that it is paired with blocking deficits with neuroanatomical lesions in the rat *Author for correspondence (e-mail: [email protected]). 2046 R. S. THORN AND B. H. SMITH amygdala. They found that neurotoxic lesions in the central Conditioning protocols nucleus of the amygdala could affect the ability of changes in Honeybees were odor-trained using the restrained bee the US to unblock mixture training, and their interpretation was preparation as described elsewhere (Kuwabara, 1957; that the amygdala was important in directing attention to novel Bitterman et al. 1983; Menzel, 1990). In brief, individual CS–US pairs. These studies all suggest that blocking involves subjects were mounted in a harness that allowed them to move several distinct brain pathways of attention and memory to the their head, antennae and mouthparts. Each was trained to CS and the US. associate a brief 4 s pulse of odor in a moving airstream with It would be useful to compare this organization with that of a touch of 2.0 mol l−1 sucrose solution to the antenna. The other systems displaying blocking. Olfactory learning in the timing of odor delivery was controlled via computer. The honeybee (Apis mellifera) displays robust blocking, as sucrose acts as a US, releasing a motor pattern called the mentioned above, and is increasingly well-characterized at the proboscis extension reflex (PER) that bees use to ingest nectar. neuroanatomical level (for reviews, see Hammer and Menzel, PER was reinforced with a 0.4 µl drop of a 2.0 mol l−1 sucrose 1995; Menzel and Muller, 1996). In brief, odor-sensitive solution in each conditioning trial. The timing of US delivery antennal sensory cells project their axons into the antennal lobe was signaled to begin 3 s after odor onset and, given the time where they end in discrete glomeruli reminiscent of the it takes to consume the 0.4 µl droplet, would extend slightly vertebrate olfactory lobe. In the antennal lobe, they synapse beyond odor delivery. A subject that has learned the CS–US with different interneurons; most are local inhibitory association will frequently exhibit PER in response to the odor interneurons that project between glomeruli, but some project alone, or prior to US onset, after as few as 1–2 conditioning out to higher brain centers, specifically the mushroom bodies trials (Menzel, 1990). and lateral protocerebral lobes (Homberg, 1984; Flanagan and The conditioning protocol for odor blocking consisted of Mercer, 1989; Fonta et al. 1993). The former region is believed three phases of training conducted in parallel on two different to be an associative center (Erber et al. 1980; Mobbs, 1985; groups of honeybees using the procedure developed for Davis, 1993; de Belle and Heisenberg, 1994), while the function honeybees by Smith and Cobey (1994; Table 1). In the of the latter is less clear, although it is thought to be a premotor pretraining phase, subjects were conditioned in a cluster of four center. Odor blocking could occur at any or all of these levels. trials with a 10 min intertrial interval (ITI) (this interval was To investigate the potential involvement of these sites in the constant across all phases). All subjects experienced one of two production of blocking, it is particularly important to determine pure odorants as the CS during this phase. Group BLOCK was what sorts of experimental manipulations attenuate blocking. exposed to the blocking odorant (A), while the control group Such information is crucial for elucidating the neural and NOVEL received the other odorant (N). In the mixture phase, behavioral mechanisms of blocking in any system. In the each subject in both groups was conditioned with a mixture of present work, experimental manipulations were designed to two odorants as the new odor CS for a block of four trials. One affect the neural representation of the CS. We used proboscis of the odors was A and the other was a new odor X. This AX extension conditioning in honeybees specifically to examine compound odor was used to train both the groups NOVEL and how the antennae and the two hemispheres of the brain interact BLOCK; however, subjects in group BLOCK were the only in olfactory learning and blocking (Smith and Cobey, 1994; ones to have experienced one of the mixture components (i.e. Smith, 1996, 1997). We show that honeybees require A) during pretraining. A 0.4 µl droplet of 2.0 mol l−1 sucrose stimulation to both antennae to facilitate blocking and that the was again used as reinforcement in both phases. dynamics of this bilateral interaction are complex. In the final test phase, each subject was presented with a series of four consecutive unreinforced (extinction) trials consisting of exposure to a 4 s pulse of odorant X on its own. Materials and methods If pretraining significantly blocked acquisition of X during the Honeybee (Apis mellifera L.) workers were obtained either mixture phase, then subjects that had experienced A in the from indoor colonies (during the months of February and pretraining phase (i.e. group BLOCK; Table 1) would be March) or from colonies maintained outdoors (April–May). We expected to show significantly fewer PER responses on specifically used foragers for all of our training to minimize any average to X across the four trials in this phase than subjects variability due to age or behavioral caste. The indoor colonies that had experienced odor N (i.e. group NOVEL; Table 1). In were maintained in a flight room on a 16 h:8 h light:dark cycle and fed unscented sucrose solutions. ‘Foraging’ honeybees Table 1. Summary of treatment groups used in blocking from the indoor colonies typically flew towards the overhead experiments lights and briefly alighted on the net.
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