1. Sensitization and classical odor conditioning of the proboscis extension reflex were functionally analyzed by repeated intracellular recordings from a single identified neuron (PE1-neuron) in the central bee brain. This neuron belongs to the class of "extrinsic cells" arising from the pedunculus of the mushroom bodies and has extensive arborizations in the median and lateral protocerebrum. The recordings were performed on isolated bee heads. 2. Two different series of physiological experiments were carried out with the use of a similar temporal succession of stimuli as in previous behavioral experiments. In the first series, one group of animals was used for a single conditioning trial [conditioned stimulus (CS), carnation; unconditioned stimulus (US), sucrose solution to the antennae and proboscis), a second group was used for sensitization (sensitizing stimulus, sucrose solution to the antennae and/or proboscis), and the third group served as control (no sucrose stimulation). In the second series, a differential conditioning paradigm (paired odor CS+, carnation; unpaired odor CS-, orange blossom) was applied to test the associative nature of the conditioning effect. 3. The PE1-neuron showed a characteristic burstlike odor response before the training procedures. The treatments resulted in different spike-frequency modulations of this response, which were specific for the nonassociative and associative stimulus paradigms applied. During differential conditioning, there are dynamic up and down modulations of spike frequencies and of the DC potentials underlying the responses to the CS+. Overall, only transient changes in the minute range were observed. 4. The results of the sensitization procedures suggest two qualitatively different US pathways. The comparison between sensitization and one-trial conditioning shows differential effects of nonassociative and associative stimulus paradigms on the response behavior of the PE1-neuron. The results of the differential conditioning procedure reveal that the effect observed for the one-trial conditioning paradigm is of an associative nature and that there might be modulations, which are specific for single and multiple trial conditioning procedures. It is hypothesized that the PE1-neuron is a possible element involved in the short-term acquisition, rather than in the long-term storage, of an associative olfactory memory in the honeybee.
Serotonin (5HT)-induced short-term facilitation and long-term facilitation (STF and LTF) of the monosynaptic connection between tail sensory neurons (SNs) and motor neurons (MNs) in Aplysia have been useful in delineating possible cellular mechanisms contributing to short-term and long-term memory. Previous work from our laboratory showed that LTF can be produced in the absence of STF, suggesting that these processes may be functionally independent. In the present study, we explored this hypothesis by examining the temporal relationship between STF and LTF. We recorded intracellularly from pairs of monosynaptically connected SNs and MNs in isolated pleural-pedal ganglia. In the first experimental series, we followed the time course of LTF across a 24 hr period after its induction by five applications of 10 M 5HT. STF completely decayed to baseline several hours before the expression of LTF. This biphasic expression profile of STF and LTF further supports the hypothesis that LTF is not a simple elaboration of STF. In the second experimental series, we monitored the immediate expression of facilitation during and after different numbers of 5HT applications. We identified a rapidly decaying STF (lasting 15-30 min) after one to four pulses of 50 M 5HT and a unique, prolonged intermediate-term facilitation (ITF; lasting up to 90 min) after five pulses of 50 M 5HT. These results raise the possibility that STF, ITF, and LTF may reflect components of different memory phases in the intact animal.
The matching behavior of honeybees in a patch of four artificial feeders was studied under two different environmental conditions in order to examine the involvement of different stimuli in the choice process. Matching fails if all nearby landmarks are removed but can, under certain conditions, be restored by subsequently introducing odors, colors, or landmarks showing that there is no unique stimulus modality that provides matching. We propose two fundamentally different memory processes, both of which affect feeding behavior and support matching. Wesuggest that in one case, the probability of choice is determined by the strength of direct associations between locally perceived odor stimuli and reward rates. In the second case, simultaneously perceived color stimuli predict the relative reward rates indirectly by the spatial representation of the four feeders. Both memory processes are likely to interact and lead to efficient feeding behavior during foraging under natural conditions. Foraging honeybees exhibit a great variety ofbehaviors, which have interested researchers for almost a century (Bitterman, 1988;Gould, 1984;Lindauer, 1963;Menzel, 1990;Opfinger, 1931;Seeley, 1989;von Frisch, 1967). Although the literature on foraging is strongly influenced by ultimate arguments and revolves around optimality criteria (Cheverton, Kacelnik, & Krebs, 1985;Kacelnik, Houston, & Schmid-Hempel, 1986), it is well known that honeybees have phenomenal learning capabilities with respect to the location, efficiency, and production cycles (timing) of different food sources (von Frisch, 1967;Gould, 1984;Heinrich, 1985;Menzel, 1990). Thus an analysis of the proximate mechanisms in the natural setting is called for. Supporting the idea that honeybees make specific use oftheir learning capabilities during foraging, Greggers and Menzel (1993) recently showed that honeybees foraging in a patch of four artificial feeding sites (feeders) matched their choice frequencies to the relative reward rates of the feeders-that is, they visited the higher rewarding feeders more frequently than the lower rewarding feeders. This applied to both "stay" flights (the bee revisits the feeder just visited) and "shift" flights (the bee chooses one ofthe three alternative feeders). Matching was first described by Herrnstein (1961) and refers to an appetitive choice behavior produced by concurrent reinforcement schedules of at least two alternatives. If the animal matches, the response rates to the We are thankful to the referees for providing many constructive criticisms. We thank T. 1. Carew, S. Fisher, M. Hammer, and R. Menzel for valuable commentary and criticism on earlier versions of the manuscript and A. Carney for essential help in preparing the English manuscript. Correspondence should be addressed to U. Greggers, Institut fur Neurobiologie, Freie Universitiit Berlin, Konigin-Luise-Str. 28-30, Berlin, Germany (e-mail: greggers@neuro.biologie.fu-berlin.de).alternatives reflect their relative reward rates (Herrnstein, 1961) or the relative amount o...
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