Long-Term Synaptic Plasticity in the Honeybee
S. Oleskevich1,
J. D. Clements2, and
M. V. Srinivasan1
1 Research School of Biological Sciences, 2 John Curtin School of Medical Research, Australian National University, Canberra ACT, 2601, Australia
 |
ABSTRACT |
Oleskevich, S., J. D. Clements, and M. V. Srinivasan. Long-term synaptic plasticity in the honeybee. J. Neurophysiol. 78: 528-532, 1997. A monosynaptic response was recorded in vivo in the mushroom body of the bee brain, an important site for memory consolidation. Focal electrical stimulation of a major afferent input evoked an extracellular field potential that consisted of a presynaptic fiber volley and a postsynaptic response. We report a long-lasting potentiation of the synaptic response (2.6-fold increase;
3.5 h). Potentiation of the response was induced by low-frequency stimulation (0.02-1.0 Hz), was input specific, and was maintained in the absence of stimulation. Paired-pulse facilitation of the response was converted to paired-pulse depression after potentiation, suggesting a presynaptic mechanism. This is the first demonstration of long-term synaptic plasticity in the insect brain.
 |
INTRODUCTION |
Long-lasting changes in synaptic transmission are thought to play a critical role in learning and memory (Bliss and Collingridge 1993
). The honeybee, with an impressive learning capacity and simple central nervous system, provides a good model for studying the basic mechanisms of memory formation. The honeybee can form a long-lasting associative olfactory memory after a single learning trial (Menzel 1990
; Sandoz et al. 1995
). It can memorize a path through a maze and learn to discriminate between complex visual patterns (Menzel 1990
; Zhang et al. 1996
). The mushroom bodies of the insect brain are the putative site of memory storage (Davis 1993
; Hammer and Menzel 1995
; Menzel 1994). Localized cooling of this structure can induce retrograde amnesia of olfactory learning (Erber et al. 1980
); genetic manipulation results in defective olfactory learning (Heisenberg et al. 1985
; Nighorn et al. 1991
; Tully and Quinn 1985
).
The anatomy of the mushroom bodies has been described in detail (Kenyon 1896
; Mobbs 1982
). The mushroom body (MB) is a bilaterally symmetrical structure consisting in total of ~340,000 neurons or about one-third of the bee brain (Witthöft 1967
). Each MB contains neurons called Kenyon cells (4-7 µm in diameter), arranged in a highly organized manner with dendrites, cell bodies, and axon terminals separated into distinct neuropils called the calyx (input region), the peduncle, and the
- and
-lobes (output region). The MB receives olfactory input, from the antennal lobe via the antenno-glomerular tracts, and visual input, from the lobula and medulla via the optic tracts (Fig. 1A) (Mobbs 1982
). The olfactory input preferentially innervates the lip and basal ring of the calyx, whereas the visual input terminates in the collar of the calyx (Mobbs 1982
).

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| FIG. 1.
Basic properties of extracellular field response in mushroom body (MB) of the honeybee. A: schematic representation of bee brain showing primary structures relevant to present experiments. A stimulation electrode (S1) in antennal lobe activated Kenyon cells in mushroom body (MB), presumably via antenno-glomerular tract (agt). A stimulation electrode (S2) in lobula (lob) also produced a response in MB, presumably via anterior superior optic tract (asot). A recording electrode was placed in center of calyx, close to Kenyon cell bodies, which fill center of the calyx, and away from their dendrites, which line calyx walls. B: orthodromic stimulation of antennal lobe (S1) evoked an extracellular field response in MB. Response was composed of a presynaptic afferent volley ( ) and a postsynaptic population spike ( ). An increase in stimulus strength elicited a population spike superimposed on a synaptic potential (inset). Stimulation artefact is blanked. Average of 80 traces. C: consecutive stimuli (S1) induced a paired-pulse facilitation of the population spike (62%) but not of afferent volley. Average of 30 traces. D: high-frequency stimulation depressed amplitude of population spike by 92% of control at 125 ms after tetanus. Amplitude of afferent volley was reduced by 13% but area remained constant suggesting a stable but less synchronous firing of presynaptic afferents (see also Fig 1C). Amplitudes are shown normalized to control values measured before tetanus. E: micropressure application of cobalt transiently attenuates amplitude of population spike by 45%, but not afferent volley. Afferent volley ( ) and population spike ( ) in all figures.
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Synaptic plasticity has frequently been studied using electrical stimulation of a presynaptic afferent pathway combined with extracellular recording of a postsynaptic field response. Electrical stimulation of the antennae has evoked synaptic responses in the MB of the cockroach and the locust (Laurent and Naraghi 1994
; Maynard 1956
), whereas in the honeybee MB, field potentials have been recorded in response to external stimuli such as light and scent (Kaulen et al. 1984
; Mercer and Erber 1983
). However, a synaptic response to focal electrical stimulation of a sensory pathway has not previously been recorded in the MB of the honeybee. Here we report that a monosynaptic response can be recorded after stimulation of the olfactory pathway. We also demonstrate that this pathway exhibits synaptic plasticity, similar in many ways to the plasticity reported in the mammalian hippocampus (Bliss and Collingridge 1993
).
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METHODS |
Experiments were carried out in vivo at room temperature (24°C) with adult foraging honeybees (n = 55). The head was secured with wax, and the brain was exposed through a small opening in the head capsule. After surgery, the bee was allowed to recover for 20-40 min before the start of the experiment.
Extracellular recordings were made with glass electrodes (0.5-1M
), filled with physiological saline containing (in mM) 140 NaCl, 5 KCl, 5 CaCl2, 14 glucose, 4 NaHCO3, 6 N-2-hydroxyethylpiperazine-N
-2-ethanesulfonic acid (pH = 7.4; Osm = 318 mOsm), and placed in the center of the median calyx at a depth of 50-150 µm. A small silver wire hooked onto the head capsule and bathed in bee hemolymph provided the ground. Focal stimulation (0.1 ms; 2-7 V) was delivered via a concentric bipolar electrode consisting of a central tungsten wire insulated by a glass pipette to within 50 µm of the tip and coated with a silver shield to provide the current return path. The exposed tip of the stimulator was positioned in the dorsomedial antennal lobe (~750 µm from the recording electrode) where the antenno-glomerular tracts originate (Mobbs 1982
). Stimulation of the antennal lobe evoked a characteristic extracellular field response in the calyx (Fig. 1B), different to that seen in exploratory recordings from other regions of the MB (peduncle and alpha-lobe). The characteristic response helped ensure accurate and reproducible placement of the recording electrode. The latency from the stimulation in the antennal lobe to the onset of the response in the calyx (2.9 ± 0.1 ms) predicted a conduction velocity of 0.25 m/s, similar to that reported in other insects (Maynard 1967
). Alternate positioning of the stimulating electrode close to the medial antenno-glomerular tract produced a response similar to that evoked by dorso-medial antennal lobe stimulation. The extracellular response in the MB could be abolished by moving the stimulating electrode to the lateral protocerebrum (a lateral movement of ~200 µm), thereby confirming focal stimulation. Stimulation of the antennal lobe did not evoke a detectable response in the contralateral MB (n = 5), which allowed separate experiments to be performed on each side of the brain.
In some experiments, a second concentric bipolar stimulating electrode was positioned in the dorsal lobula, close to the origin of the anterior superior optic tract. In other experiments, paired pulses were evoked by two consecutive stimuli to the antennal lobe separated by 20 ms (Fig. 1C) or 22.5 ms (Fig. 3C). High-frequency stimulation consisted of 10 stimulations at 100 Hz. Micropressure injection of cobalt (20 mM) or cadmium (1-10 mM) was delivered through the recording electrode (2-5 nl). Synaptic responses were measured 2-5 min after injection to allow for drug diffusion and mechanical stabilization. Amplitudes were measured from a sloping line connecting the two maxima immediately before and after the response (population spike or afferent volley). If the volley amplitude changed by >15% during the course of the experiment, the results were not used.

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| FIG. 3.
Induction of long-lasting potentiation was independent of stimulus frequency. A: amplitude of population spike potentiated with either 0.2 or 0.02 Hz stimulation. B: rate of potentiation per minute at 0.1 Hz (46 ± 5%; n = 9) was significantly greater than the rate at 0.02-0.05 Hz (26 ± 9%; n = 6), rate at 0.2-0.5 Hz (24 ± 8%; n = 5), and rate at 1.0 Hz(20 ± 8%; n = 4). Percent potentiation per stimulus at 0.02-0.05 Hz stimulation (20 ± 7%) was significantly greater than that at 0.1 Hz (8 ± 1%), at 0.2-0.5 Hz (1 ± 0.5), and at 1 Hz (0.3 ± 0.1). C: fraction of experiments that showed a potentiation in first 5 min of recording was similar for stimulation frequencies of 0.02-0.05 Hz (1.0), 0.1 Hz (0.75 ± 0.13), 0.2-0.5 Hz (0.71 ± 0.17), and 1 Hz (0.80 ± 0.18). Total number of experiments for each group is given in parentheses.
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The rate of potentiation (percent potentiation/minute or stimulus) was an average rate calculated during 5 min from the onset of stimulation. The fraction potentiated is the number of responses that potentiated (>15%) after 5 min compared with the total number of experiments. Measures are expressed as means ± SE, except in Fig. 3C where the error bars show SD as calculated from the binomial distribution. Statistical analyses were performed with a two-tailed t-test with significance levels as indicated.
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RESULTS |
Basic response
Extracellular field potentials were recorded in vivo in the MB calyx, after focal stimulation of the antennal lobe, a region analogous to the vertebrate olfactory lobe (Fig. 1A). As elucidated below, the field potential consisted of a presynaptic afferent fiber volley followed by a postsynaptic potential. An increase in stimulus strength elicited a population spike superimposed on the synaptic potential (Fig. 1B, inset; n = 7). The mean amplitudes of the afferent volley and population spike were 1.1 ± 0.1 mV and 1.3 ± 0.2 mV, respectively (n = 14). The latency from the onset of stimulation was 2.9 ± 0.1 ms for the afferent volley and 8.3 ± 0.2 ms for the population spike (n = 14).

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| FIG. 2.
Induction, maintenance, and input specificity of long-lasting potentiation. A: amplitude of population spike was potentiated by 140% with low-frequency stimulation (0.1 Hz) in antennal lobe. Potentiation showed a gradual onset and saturation. Afferent volley remained stable. Representative traces averaged at 3 and 40 min are shown in inset. B: potentiated population spike amplitude was maintained for 1.75 h after intervals of no stimulation (10, 20, and 30 min). C: paired-pulse facilitation (i) evoked by consecutive stimuli in control conditions was reversed to paired-pulse depression (ii) after potentiation. Average of 10 traces for individual experiment. Summary data (bar graph) shows that ratio of amplitude of consecutive population spikes (P1 and P2) was decreased from 2.1 to 0.8 after potentiation. D: potentiation was input specific as population spike evoked by stimulation of lobula ( , S2 in Fig. 1A) was not affected ( 19%) during potentiation of antennal lobe pathway (S1; 184%). Antennal and lobula pathway were confirmed as independent before testing for input specificity (see text). S1 amplitudes were 3 point filtered.
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The identities of the putative pre- and postsynaptic components of the MB field potential were confirmed in three different ways. First, two consecutive stimuli induced a paired-pulse facilitation of the population spike (72 ± 13%) without affecting the amplitude of the afferent volley(
11 ± 5%; n = 7; Fig. 1C). Second, high-frequency stimulation fatigued the population spike without depressing the afferent volley (n = 4; Fig. 1D). The amplitude of the population spike recovered fully at ~5 s after the high-frequency stimulation paradigm. Third, micropressure injection of cobalt or cadmium into the MB reversibly attenuated the amplitude of the population spike by 42 ± 5% without affecting the afferent volley (
2 ± 1%; n = 7; Fig. 1E). Cobalt and cadmium are calcium channel blockers that inhibit neurotransmitter release and the postsynaptic response without affecting the sodium channel dependent presynaptic volley (Hille 1992
). Thus the field potential recorded in the MB consists of a presynaptic afferent fiber volley followed by a postsynaptic potential with a superimposed population spike.
Long-term synaptic plasticity
Low-frequency stimulation in the antennal lobe (0.02-1.0 Hz) induced a slowly developing long-lasting potentiation of the population spike in 24 out of 31 recordings. Potentiation was defined as a
15% or greater increase in the amplitude of the population spike after 5 min of stimulation, which persisted for the remainder of the recording (
3.5 h). The amplitude of the population spike potentiated by 80 ± 11% after 5 min of stimulation (20-240%, n = 26; P < 0.001; Fig. 2A). The potentiation was maintained in the absence of stimulation (n = 4; Fig. 2B). It reached saturation at5-25 min after the onset of continuous stimulation (165 ± 22%; n = 18; Fig. 2A). The slope of the rising phase of the population excitatory postsynaptic potential (EPSP) also potentiated but this was difficult to quantify due to partial merging of this component with the afferent volley. In those experiments where the afferent volley was sufficiently separated, the rising slope of the EPSP potentiated by 229 ± 77 % (n = 7; P < 0.005). The afferent volley remained constant in amplitude throughout the experiments, confirming stable stimulus strength and recording position. Stimulus protocols that reliably induce long-term potentiation (LTP) in the rat hippocampus (12 pulses at 100 Hz; repeated 6 times), did not produce any short- or long-term potentiation of the synaptic response in the honeybee (n = 13).
Paired-pulse facilitation (PPF) is a well-studied form of short-term synaptic plasticity that is known to be mediated by presynaptic mechanisms. A decrease in PPF can be associated with an increase in the probability of neurotransmitter release (Manabe et al. 1993
). In the mammalian hippocampus, induction of LTP often is accompanied by changes in PPF, implying the participation of presynaptic mechanisms in the potentiation process (Kuhnt and Voronin 1994
; Schulz et al. 1994
). In the present study, PPF was decreased in all cases after potentiation and was converted to paired-pulse depression (PPD) in four out of six experiments (Fig. 2C). This dramatic reduction in PPF (from 111 ± 19% to
18 ± 15%; n = 6; P < 0.001) suggests that a presynaptic mechanism contributes to the long-lasting potentiation.
To determine if the potentiation was specific to the pathway being stimulated, a second nonstimulated pathway was monitored. A stimulating electrode was placed in the lobula (S2), a region analogous to the vertebrate visual cortex (O'Carroll 1993
; Srinivasan et al. 1993
) (Fig. 1A). We first established that the two input pathways were independent (n = 10; data not shown). Paired pulses were applied to the antennal lobe pathway and PPF of the population spike was observed. Then two pulses were consecutively applied to the antennal lobe and the lobula with the same temporal separation as the paired-pulses. An absence of facilitation in the lobula response revealed that the antennal lobe and lobula provide independent pathways to the MB. In separate experiments, the lobula response showed PPF (n = 3) and potentiation with low-frequency stimulation (0.1 Hz; n = 4). Antennal lobe stimulation (0.1 Hz) potentiated the population spike by 105 ± 29% (n = 4) but produced no change in the lobula response (
8 ± 13%, n = 4; Fig. 2D). The potentiation therefore represents an increase in the efficiency of synaptic transmission, specific to the stimulated pathway.
Induction of plasticity
In the mammalian brain, synaptic plasticity can be bidirectional: it can lead to potentiation or depression depending on the frequency of stimulation (Bliss and Collingridge 1993
; Linden and Connor 1995
). In the present study, the population spike was potentiated at all stimulation frequencies tested (Fig. 3). The hypothesis that the potentiation simply integrates the number of stimuli can be ruled out because the potentiation per stimulus was strongly dependent on stimulus frequency (Fig. 3B). In contrast, the potentiation per minute was weakly dependent on stimulation frequency with a maximum potentiation rate at 0.1 Hz (Fig. 3B). The fraction of experiments showing a potentiation in the first 5 min of continuous stimulation was similar for all stimulation frequencies tested (Fig. 3C). These results suggest that the potentiation is dependent primarily on the duration of stimulation and only weakly on the frequency of stimuli.
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DISCUSSION |
Extracellular field recordings were made from the MB of the honeybee brain after electrical stimulation of the olfactory input pathway. This is the first report of such recordings, and the multicomponent field response was characterized in three separate experiments. It consisted of a negative polarity afferent volley followed by a positive polarity EPSP with a superimposed negative polarity population spike. The EPSP and population spike resemble those seen in the mammalian hippocampus. The characteristic polarities of the EPSP and population spike are consistent with the recording electrode placement in the center of the calyx, close to the densely packed Kenyon cell bodies, but away from the lip and basal ring where the olfactory inputs terminate (Mobbs 1982
). Direct electrical stimulation of the olfactory pathway is nonphysiological and is expected to produce a different response than would a natural olfactory stimulus. In the locust MB, odor presentation produces oscillatory field potentials rather than population spikes (Laurent 1996
). However, our experimental paradigm permits a direct study of plasticity at a monosynaptic connection in the MB. It also permits useful comparisons of synaptic plasticity in other preparations where similar paradigms have been employed.
The long-lasting synaptic potentiation observed in the honeybee MB is similar to the phenomenon of LTP in the mammalian hippocampus. It exhibits input specificity, maintenance in the absence of stimulation, and a presynaptic mechanism as one of its sites of action. Specifically, the conversion of PPF to PPD after potentiation strongly suggests that the probability of transmitter release has increased (Manabe et al. 1993
). The potentiation differs from LTP in that low-frequency stimulation does not result in a stable baseline amplitude for the population spike and that brief high-frequency stimulation is ineffective at inducing potentiation (Bliss and Collingridge 1993
). The absence of a stable baseline could be explained if a single stimulus produced sufficient synchronous excitation in the MB to initiate synaptic plasticity. Reducing the stimulus strength may decrease synchronous excitation and produce a stable baseline, but the extracellular field response would no longer be detectable. Alternatively, the stimulus may activate concurrently octopamine-releasing fibers that innervate and pass through the antennal lobe and terminate in the MB calyces. Octopamine has been implicated in olfactory learning and, like other monoamines, may modulate synaptic plasticity (Hammer 1993
; Hopkins and Johnston 1984
; Villani and Johnston 1993
). In mammalian preparations, different stimulation frequencies have been reported to produce different forms of synaptic plasticity. The dynamic properties of the bee synaptic potentiation, such as the gradual onset (5-20 min) and induction by low-frequency stimulation (0.02-1.0 Hz), resembled those of mammalian long-term depression, which is evoked by 7-15 min of 1-3 Hz stimulation (Linden and Connor 1995
). The optimum rate for stimulating the olfactory pathway was one stimulus every 10 s, and significant potentiation was typically achieved after 5 min. It is interesting to note that a foraging honeybee visits a flower and receives an olfactory stimulus every 11 ± 3 s (n = 8; field observations for bees foraging on Obelia grandiflora). Flower visit frequencies >0.1 Hz are unlikely due to an8-s minimun per visit (Gould and Gould 1995
).
Our study reports the long-lasting potentiation of a monosynaptic connection in the insect brain. This phenomenon is similar to long-term potentiation in vertebrates and reinforces the analogy between the role of the MB in insects and the hippocampus in vertebrates, with regard to induction and consolidation of memory. It also may provide a suitable preparation for monitoring synaptic potentiation in an actively learning animal.
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ACKNOWLEDGEMENTS |
The authors are grateful to Dr. J. M. Bekkers for useful discussions and comments on the manuscript.
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FOOTNOTES |
Address for reprint requests: S. Oleskevich, Visual Sciences, Research School of Biological Sciences, Australian National University, Canberra ACT 2601 Australia.
E-mail: Sharon.Oleskevich{at}anu.edu.au
Received 30 January 1997; accepted in final form 17 April 1997.
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