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. 2011 Apr 26;6(4):e19301.
doi: 10.1371/journal.pone.0019301.

Dance type and flight parameters are associated with different mushroom body neural activities in worker honeybee brains

Taketoshi Kiya  1 , Takeo Kubo
Affiliations

Dance type and flight parameters are associated with different mushroom body neural activities in worker honeybee brains

Taketoshi Kiya et al. PLoS One. .

Abstract

Background: Honeybee foragers can transmit the information concerning the location of food sources to their nestmates using dance communication. We previously used a novel immediate early gene, termed kakusei, to demonstrate that the neural activity of a specific mushroom body (MB) neuron subtype is preferentially enhanced in the forager brain. The sensory information related to this MB neuron activity, however, remained unclear.

Methodology/principal findings: Here, we used kakusei to analyze the relationship between MB neuron activity and types of foraging behavior. The number of kakusei-positive MB neurons was higher in the round dancers that had flown a short distance than in the waggle dancers that had flown a long distance. Furthermore, the amount of kakusei transcript in the MBs inversely related to the waggle-phase duration of the waggle dance, which correlates with the flight distance. Using a narrow tunnel whose inside was vertically or axially lined, we manipulated the pattern of visual input, which is received by the foragers during flight, and analysed kakusei expression. The amount of kakusei transcript in the MBs was related to the foraging frequency but not to the tunnel pattern. In contrast, the number of kakusei-positive MB neurons was affected by the tunnel patterns, but not related to foraging frequency.

Conclusions/significance: These results suggest that the MB neuron activity depends on the foraging frequency, whereas the number of active MB neurons is related to the pattern of visual input received during foraging flight. Our results suggest that the foraging frequency and visual experience during foraging are associated with different MB neural activities.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Round dancers have a greater number of active MB neurons than the waggle dancers.
(A and B) Schematic drawings of the rostral (A) and caudal (B) hemispheres of the worker honeybee brain. The brain regions in which signals were counted are shown in different colors. (C) Quantification data of kakusei-signal densities in various brain regions of the round and waggle dancers. Expression of kakusei was detected by in situ hybridization using coronal brain sections. A significant difference in kakusei expression between the dancers was detected in the MB neurons. There was no significant difference between the right and left hemispheres for any brain region (P>0.05). All data are represented as the mean ± standard error. Asterisks indicate P<0.05 calculated by the two-factor ANOVA. (D and E) Representative images of in situ hybridization of kakusei in the calyces of the MBs of the round and waggle dancers, respectively. The corresponding brain region is shown as a blue square in A. Some of the kakusei signals are indicated by red arrowheads. Scale bars: 100 µm. Abbreviations: AL, antennal lobe; Class II KCs, class II Kenyon cells; DL, dorsal lobe; dOL, dorsal OL; lKCs, large-type Kenyon cells MB, mushroom body; OL, optic lobe; PL, protocerebral lobe; ; sKCs, small-type Kenyon cells; vOL, ventral OL.
Figure 2
Figure 2. The amount of kakusei transcript in the brains of waggle dancers inversely correlates with the waggle-phase duration.
The relative amount of kakusei transcript was quantified by real-time RT-PCR and plotted against the waggle-phase duration. The MBs (A) and OLs (B) are indicated. The logarithmic regression lines are shown. The R2 and P values for the regression lines are shown. Note that the slope of the MBs is steeper than that of the OLs.
Figure 3
Figure 3. The amount of kakusei transcript in the brain correlates to the foraging frequency of the foragers.
(A) The probabilities of waggle or round dances. The left panel shows the data from the vertically-lined tunnel, and right panel shows the data from the axially-lined tunnel. In each tunnel experiment, the dance probabilities were compared between the tunnel and entrance groups. n indicates the number of dances analyzed. *: P<0.0001, χ2 test. N.S.: not significant. (B) The relative amount of kakusei transcript was quantified by real-time RT-PCR and compared between the tunnel and entrance groups. Left and right panels show data from the vertically- and axially-lined tunnels, respectively. Data from the MBs and OLs are shown separately. (C) and (D) The relative amount of kakusei transcript was plotted against the number of visits to the feeder during 1 hr. Data from the vertically-lined tunnels (C) and axially-lined tunnels (D) are shown. The tunnel and entrance groups were shown left and right panels, respectively. Note the robust increase in kakusei expression in the MBs. The R and P values for each regression line are shown.
Figure 4
Figure 4. A greater number of MB neurons were kakusei-positive in the foragers that flew in the vertically-lined tunnel than in those that flew the axially-lined tunnel.
The kakusei-signal densities in the MBs were compared between foragers that flew in the differently-patterned tunnels. *: P<0.05, two-factor ANOVA.
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