QUICK SEARCH:   [advanced] Author: Keyword(s):
Home     Help     Feedback     Subscriptions     Archive     Search     Table of Contents

First published online November 4, 2005
Journal of Experimental Biology 208, 4317-4332 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01908

This Article Summary Full Text Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Menzel, R. Articles by Manz, G. Search for Related Content PubMed PubMed Citation Articles by Menzel, R. Articles by Manz, G.

Neural plasticity of mushroom body-extrinsic neurons in the honeybee brain

Randolf Menzel^* and Gisela Manz

Freie Universität Berlin, Institut für Biologie-Neurobiologie, Koenigin-Luise-Strasse 28/30, D-14195 Berlin, Germany

View larger version (15K): [in a new window]   Fig. 1. Two representative examples of paired-pulse depression. (A) An unidentified alpha lobe-extrinsic neuron. All double-pulse values are significantly different from the single pulse value (P<0.001, post hoc tests, main effect: F=33, d.f.=3, P<0.001, N=43, values are means ± S.D.). (B) A PE1 neuron. All values are significantly different from the single-pulse value (*P<0.001, post hoc tests, main effect: F=55.38, d.f.=4, P<0.001, N=43, values are means ± S.D.). (C) Spike train recorded from the neuron in A. Interval between the two pulses = 30 ms. The stimulus artefacts mark the test pulses. The ordinate gives the number of spikes elicited by a single stimulus, and the abscissa plots the interval t between the two stimuli in the paired-pulse protocol.

View larger version (18K): [in a new window]   Fig. 2. Two representative examples of paired-pulse facilitation. (A) An unidentified alpha lobe-extrinsic neuron. The value for 20 ms is significantly different from all other values (*P<0.01, post hoc test, main effect: F=5.66, d.f.=3, *P<0.01, N=45, values are means ± S.D.). (B) A PE1 neuron. The value for 15 ms is significantly different from all other values (P<0.001, post hoc test, main effect: F=13.27, d.f.=3, *P<0.001, N=28). The ordinate gives the number of spikes elicited by a single stimulus. The abscissa gives the interval (t) between the two stimuli in the paired-pulse protocol. (C) Spike trains from the PE1 neuron in B. (D) Spike train from a different PE1 neuron, which was stimulated with higher-pulse currents eliciting more spikes per stimulus. The stimulus artefacts mark the test pulses.

View larger version (19K): [in a new window]   Fig. 3. Cumulative paired-pulse facilitation from an unidentified alpha lobe-extrinsic neuron (A,B) or a PE1 neuron (C). t was set to the optimal time interval of the two pulses for the induction of paired-pulse facilitation (30 ms in A, 20 ms in C). Filled circles, spike numbers elicited by the first pulse; open circles, spike numbers to the second pulse. The ordinate gives the number of spikes elicited by a single stimulus, and the abscissa time in s. In B the stimulus artefacts mark the test pulses.

View larger version (15K): [in a new window]   Fig. 4. (A) Tetanus-induced short-term depression followed by lasting augmentation. Depression induced in this unidentified alpha lobe-extrinsic neuron lasted for about 30 s and was followed by augmentation. Similar time courses of depression and augmentation were seen in three other neurons; none was identified as a PE1 neuron. (B) Spike trains of this neuron 70 s after tetanus. The stimulus artefacts mark the test pulses. (C) Average time course of depression in five PE1 neurons. Notice the different time scale in A and C. The ordinates give the number of spikes elicited by a single stimulus (± S.D. in C.) and the abscissa time in s (A) or min (C).

View larger version (12K): [in a new window]   Fig. 5. (A) Tetanus-induced augmentation in an A5 alpha lobe-extrinsic neuron. The neuron was identified by intracellular marking and categorized according to Rybak and Menzel (1993). The augmentation effect was very constant in three consecutive tetani, and the neuron returned to its initial sensitivity within 1 min. Therefore, the responses to test stimuli shortly before and after the three tetani were overlaid in the figure. (B) Spike trains of the neuron in A recorded at two intervals after the first tetanus (arrows). The stimulus artefacts mark the test pulses. (C) Augmentation of 11 PE1 neurons. The ordinates give the number of spikes elicited by a single stimulus (± S.D. C), and the abscissa time in s.

View larger version (20K): [in a new window]   Fig. 6. Reduction (A,B) and enhancement (C) of tetanus-induced augmentation after repeated tetani. Both neurons were unidentified alpha lobe-extrinsic neurons. The tetani (T in A; thick vertical lines in B,C) were repeated at intervals of 1–2 min. In A,B, four tetani were applied (the second tetanus is not shown in the diagrams in B but can be seen in the spike frequency plot in A). In C, three tetani were applied. (A) Spontaneous and stimulus-induced spike frequency shown as a dot plot (instantaneous frequency). The neuron had a tendency to produce short bursts at intervals of about 10 s. This form of bursting behaviour became more prominent after the fourth tetanus. Test stimuli were given at 1 s intervals. The ordinates in B and C show the number of spikes elicited by a single stimulus, and the abscissa time in min.

View larger version (13K): [in a new window]   Fig. 7. Mechanistic relationship between paired-pulse facilitation and tetanus-induced augmentation for (A,B) a A5-3 neuron, a type of neuron MB-extrinsic neuron that was characterized with respect to its branching pattern and the location of its soma by Rybak and Menzel (1993), and (C) a PE1 neuron. (A,B) The A5-3 neuron was first stimulated by repeated paired pulses with pulse intervals of 30 ms, then a tetanus (thick vertical line) was applied and the paired pulses were continued (A). Afterwards the neuron was stimulated with paired pulses with pulse intervals of 60 ms, then a tetanus was applied, followed by a continuation of paired-pulse stimuli (B). Before the tetanus the paired pulses caused a slight facilatory effect with little difference between the repeated paired pulses of 30 ms and 60 ms. Responses to the second pulse facilitated after the tetanus in the t=30 ms protocol, but not in the t=60 ms protocol. (C) The PE1 neuron was first stimulated with paired pulses at intervals of 30 ms, then tetanus was applied. The facilatory effect of the tetanus is expressed in the responses to both the first and the second pulse, and no change is found between paired pulse facilitation before and after the tetanus. Filled circles, number of spikes for the first stimulus in the paired pulses; open circles, those for the second stimulus. The ordinate in the diagrams gives the number of spikes elicited by a single stimulus, and the abscissa time in s.

View larger version (27K): [in a new window]   Fig. 8. Site-specificity of tetanus-induced plasticity in alpha lobe-extrinsic neurons. (A) Each MB consists of two halves. One half is composed of K-cells with their somata and dendrites in the median calyx (m), and another half has somata and dendrites in the lateral calyx (l). The axons of the K-cells fuse in the peduncle and send their collaterals into the alpha lobe (). There the lateral and the median sectors house the axon collaterals of the respective calyces. All alpha lobe-extrinsic neurons that we marked in the course of our study branched across the whole alpha lobe, making it very likely that they receive input from both median and lateral K-cells. (B) This Pe1 neuron responded with depression after tetanus to the lateral calyx. Depression was found for the test stimuli to both the median (filled triangles) and the lateral calyx (open triangles). The delayed augmentation effect, however, was site-specific. Only the input from the tetanized calyx augmented. (C,D) Two examples from unidentified alpha lobe-extrinsic neurons for site-specific facilitation induced by tetanus. Again the tetanus was applied to the lateral calyx, and the responses to test stimuli in the median (filled triangles) and lateral (open triangles) were monitored during successive minutes. The ordinate in the diagrams gives the number of spikes elicited by a single stimulus, and the abscissa time in min. The stimulus artefacts in B, C and D mark the test pulses.

View larger version (36K): [in a new window]   Fig. 9. Long-term potentiation induced in two PE1 neurons (A,B) by pairing tetanus to the K-cells with simultaneously depolarizing the PE1 neuron. The broken lines indicates a tetanus, dotted lines a tetanus paired with hyper-polarization of the PE1 neuron, and bold lines a tetanus paired with depolarization. Test stimuli were applied at intervals of 20 s. The stimulus artefacts mark the test pulses. (Ai,Bi) The results for the amplitude of summed EPSPs in mV. The maximum of the dc component was measured as EPSP amplitude. Eight consecutive test stimuli were averaged. (Aii,Bii) Mean of the number of spikes to eight consecutive test stimuli. Values are means ± S.D.; box, S.E.M. Where only filled circles are shown all eight values were the same. Notice the draught about 20 min after the pairing of the tetanus with depolarization (see text). The ordinate gives the dc amplitude (Ai,Bi) and number of spikes (Aii,Bii) elicited by a single stimulus, and the abscissa time in min (notice the different scales in the two graphs, and the high value of summed EPSPs before the application of a tetanus in the neuron of A).

View larger version (23K): [in a new window]   Fig. 10. Structural correlates of the inputs from the K-cells to the PE1 neuron. (A) High resolution camera lucida drawing of the two spiny regions of the PE1 dendrites; (Ai) finger-like spiny terminals of the dendrites in the region deep in the peduncle, (Aii) spiny branches at the base of the PE1 close to the integrating segment of the dendrites. Scale bar, 10 µm. (B) Scheme of the two spiny regions of the PE1 dendrites in the finger-like branches that make contact with K-cell axons from the three calyx regions, lip (li), collar (co), basal ring (br), and those in the region of the ventral alpha lobe (ventr. -L).