Detection of Neural Activity in the Brains of Japanese Honeybee Workers during the Formation of a “Hot Defensive Bee Ball”
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{"title"=>"Detection of neural activity in the brains of japanese honeybee workers during the formation of a \"Hot defensive bee ball\"", "type"=>"journal", "authors"=>[{"first_name"=>"Atsushi", "last_name"=>"Ugajin", "scopus_author_id"=>"39162248900"}, {"first_name"=>"Taketoshi", "last_name"=>"Kiya", "scopus_author_id"=>"23479927900"}, {"first_name"=>"Takekazu", "last_name"=>"Kunieda", "scopus_author_id"=>"7103260718"}, {"first_name"=>"Masato", "last_name"=>"Ono", "scopus_author_id"=>"36133626800"}, {"first_name"=>"Tadaharu", "last_name"=>"Yoshida", "scopus_author_id"=>"22956374700"}, {"first_name"=>"Takeo", "last_name"=>"Kubo", "scopus_author_id"=>"35227541600"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84858259323", "scopus"=>"2-s2.0-84858259323", "doi"=>"10.1371/journal.pone.0032902", "isbn"=>"1932-6203", "pui"=>"364433907", "issn"=>"19326203", "pmid"=>"22431987"}, "id"=>"031c4728-dd17-3492-a77b-47aa5b71c452", "abstract"=>"Anti-predator behaviors are essential to survival for most animals. The neural bases of such behaviors, however, remain largely unknown. Although honeybees commonly use their stingers to counterattack predators, the Japanese honeybee (Apis cerana japonica) uses a different strategy to fight against the giant hornet (Vespa mandarinia japonica). Instead of stinging the hornet, Japanese honeybees form a \"hot defensive bee ball\" by surrounding the hornet en masse, killing it with heat. The European honeybee (A. mellifera ligustica), on the other hand, does not exhibit this behavior, and their colonies are often destroyed by a hornet attack. In the present study, we attempted to analyze the neural basis of this behavior by mapping the active brain regions of Japanese honeybee workers during the formation of a hot defensive bee ball. First, we identified an A. cerana homolog (Acks = Apis cerana kakusei) of kakusei, an immediate early gene that we previously identified from A. mellifera, and showed that Acks has characteristics similar to kakusei and can be used to visualize active brain regions in A. cerana. Using Acks as a neural activity marker, we demonstrated that neural activity in the mushroom bodies, especially in Class II Kenyon cells, one subtype of mushroom body intrinsic neurons, and a restricted area between the dorsal lobes and the optic lobes was increased in the brains of Japanese honeybee workers involved in the formation of a hot defensive bee ball. In addition, workers exposed to 46°C heat also exhibited Acks expression patterns similar to those observed in the brains of workers involved in the formation of a hot defensive bee ball, suggesting that the neural activity observed in the brains of workers involved in the hot defensive bee ball mainly reflects thermal stimuli processing.", "link"=>"http://www.mendeley.com/research/detection-neural-activity-brains-japanese-honeybee-workers-during-formation-hot-defensive-bee-ball", "reader_count"=>54, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>5, "Researcher"=>13, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>4, "Student > Master"=>12, "Other"=>2, "Student > Bachelor"=>3, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>5, "Researcher"=>13, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>4, "Student > Master"=>12, "Other"=>2, "Student > Bachelor"=>3, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Agricultural and Biological Sciences"=>34, "Philosophy"=>1, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>1, "Computer Science"=>3, "Engineering"=>2, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>5, "Medicine and Dentistry"=>1, "Neuroscience"=>1, "Psychology"=>2, "Social Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Psychology"=>{"Psychology"=>2}, "Unspecified"=>{"Unspecified"=>1}, "Environmental Science"=>{"Environmental Science"=>1}, "Engineering"=>{"Engineering"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Neuroscience"=>{"Neuroscience"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>34}, "Computer Science"=>{"Computer Science"=>3}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Philosophy"=>{"Philosophy"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"United States"=>1, "Japan"=>3, "Switzerland"=>1, "Germany"=>2}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/342800", "https://ndownloader.figshare.com/files/342872", "https://ndownloader.figshare.com/files/342948", "https://ndownloader.figshare.com/files/343001"], "description"=>"<div><p>Anti-predator behaviors are essential to survival for most animals. The neural bases of such behaviors, however, remain largely unknown. Although honeybees commonly use their stingers to counterattack predators, the Japanese honeybee (<em>Apis cerana japonica</em>) uses a different strategy to fight against the giant hornet (<em>Vespa mandarinia japonica</em>). Instead of stinging the hornet, Japanese honeybees form a “hot defensive bee ball” by surrounding the hornet <em>en masse</em>, killing it with heat. The European honeybee (<em>A. mellifera ligustica</em>), on the other hand, does not exhibit this behavior, and their colonies are often destroyed by a hornet attack. In the present study, we attempted to analyze the neural basis of this behavior by mapping the active brain regions of Japanese honeybee workers during the formation of a hot defensive bee ball. First, we identified an <em>A. cerana</em> homolog (<em>Acks</em> = <em><u>A</u>pis <u>c</u>erana <u>k</u>aku<u>s</u>ei</em>) of <em>kakusei</em>, an immediate early gene that we previously identified from <em>A. mellifera</em>, and showed that <em>Acks</em> has characteristics similar to <em>kakusei</em> and can be used to visualize active brain regions in <em>A. cerana</em>. Using <em>Acks</em> as a neural activity marker, we demonstrated that neural activity in the mushroom bodies, especially in Class II Kenyon cells, one subtype of mushroom body intrinsic neurons, and a restricted area between the dorsal lobes and the optic lobes was increased in the brains of Japanese honeybee workers involved in the formation of a hot defensive bee ball. In addition, workers exposed to 46°C heat also exhibited <em>Acks</em> expression patterns similar to those observed in the brains of workers involved in the formation of a hot defensive bee ball, suggesting that the neural activity observed in the brains of workers involved in the hot defensive bee ball mainly reflects thermal stimuli processing.</p> </div>", "links"=>[], "tags"=>["detection", "neural", "brains", "japanese", "honeybee", "workers"], "article_id"=>127764, "categories"=>["Neuroscience", "Evolutionary Biology"], "users"=>["Atsushi Ugajin", "Taketoshi Kiya", "Takekazu Kunieda", "Masato Ono", "Tadaharu Yoshida", "Takeo Kubo"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0032902.s001", "https://dx.doi.org/10.1371/journal.pone.0032902.s002", "https://dx.doi.org/10.1371/journal.pone.0032902.s003", "https://dx.doi.org/10.1371/journal.pone.0032902.s004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Detection_of_Neural_Activity_in_the_Brains_of_Japanese_Honeybee_Workers_during_the_Formation_of_a_Hot_Defensive_Bee_Ball_/127764", "title"=>"Detection of Neural Activity in the Brains of Japanese Honeybee Workers during the Formation of a “Hot Defensive Bee Ball”", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-03-14 02:09:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/667301"], "description"=>"<p>(A) Overview of <i>Acks</i> cDNA and open reading frame (ORF) analysis. The yellow bar and black bar represent the <i>Acks</i> cDNA region highly conserved among the <i>Acks</i> and <i>kakusei</i> cDNAs and the region adjacent to the <i>Acks</i> cDNA, respectively. The arrow indicates the region corresponding to the putative neural activity-inducible <i>Acks</i> transcript. The orange bar indicates the region corresponding to sense and antisense probes used in the <i>in situ</i> hybridization. Horizontal boxes under the upper yellow and black bar indicate open reading frame analysis in each reading frame of the <i>Acks</i> cDNA, respectively. The blue and pink bars present in each box indicate positions of initiation and termination codons, respectively. Colored squares on the horizontal boxes indicate potential ORFs longer than 150b. The blue (in Frame 1) and red box (in Frame 1) indicate the longest ORF and the ORF conserved among <i>Acks</i> and <i>kakusei</i> cDNAs, respectively. (B) Time course of <i>Acks</i> expression level investigated by quantitative RT-PCR after seizure induction under room temperature (25°C). Values are means ± SEM (a, different from 0 min <i>P</i><0.01; b, different from 30 min <i>P</i><0.01; c, different from 45 min <i>P</i><0.01; d, different from 60 min <i>P</i><0.01; Tukey-Kramer's test). Sz-induced, seizure-induced. (C) Time course of <i>Acks</i> expression level investigated by quantitative RT-PCR after seizure induction under the high temperature (46°C). Values are means ± SEM (a, different from 0 min <i>P</i><0.01; b, different from 15 min <i>P</i><0.05; c, different from 90 min <i>P</i><0.01; d, different from 150 min <i>P</i><0.05; Tukey-Kramer's test).</p>", "links"=>[], "tags"=>["characterization", "japanese", "honeybee", "non-coding"], "article_id"=>337785, "categories"=>["Neuroscience", "Evolutionary Biology"], "users"=>["Atsushi Ugajin", "Taketoshi Kiya", "Takekazu Kunieda", "Masato Ono", "Tadaharu Yoshida", "Takeo Kubo"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0032902.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_and_characterization_of_Acks_the_Japanese_honeybee_kakusei_homolog_as_a_non_coding_IEG_/337785", "title"=>"Identification and characterization of <i>Acks</i>, the Japanese honeybee <i>kakusei</i> homolog, as a non-coding IEG.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-14 02:09:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/667450"], "description"=>"<p>(A) Schematic diagram of the lateral view of a bee brain. Areas colored in light orange indicate neuropil regions. D, dorsal; V, ventral; R, rostral; C, caudal. MB, mushroom bodies; AL, antennal lobes; and SOG, subesophageal ganglion. The green line indicates the position of sections analyzed in this experiment. (B) A schematic diagram of a middle right brain hemisphere of the Japanese worker honeybee. Areas colored in light grey indicate brain areas where the somata of neurons are located. Red squares correspond to brain areas whose <i>in situ</i> hybridization results are presented below. M, medial; L, lateral. OL, optic lobe; DL, dorsal lobe. (C–N) Expression analysis of <i>Acks</i> by <i>in situ</i> hybridization using coronal brain sections of seizure-induced (Sz-induced) (C–H) or control Japanese honeybee workers (I–N). The upper panels (C and I), middle panels (E and K), and lower panels (G and M) correspond to MB, OL, and area between the DL and OL, which are boxed in (B). Bars indicate 100 µm. (D, F, H, J, L, and N) Magnified views of the regions delineated by dotted lines in panels (C), (E), (G), (I), (K), and (M), respectively. Yellow arrowheads indicate <i>Acks</i> signals. Bars indicate 10 µm.</p>", "links"=>[], "tags"=>["neural", "brains", "japanese", "honeybee"], "article_id"=>337934, "categories"=>["Neuroscience", "Evolutionary Biology"], "users"=>["Atsushi Ugajin", "Taketoshi Kiya", "Takekazu Kunieda", "Masato Ono", "Tadaharu Yoshida", "Takeo Kubo"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0032902.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Seizure_induced_neural_activity_in_the_brains_of_the_Japanese_honeybee_workers_/337934", "title"=>"Seizure-induced neural activity in the brains of the Japanese honeybee workers.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-14 02:12:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/667600"], "description"=>"<p>(A) Presentation of a wire-hung hornet to the beehive as a decoy. (B) Hundreds of workers form a hot defensive bee ball surrounding the wire-hung giant hornet. (C) Bee ball recovered in a glass beaker. (D) The giant hornet is dead 60 min after the bee ball forms.</p>", "links"=>[], "tags"=>["workers", "artificially", "formed"], "article_id"=>338085, "categories"=>["Neuroscience", "Evolutionary Biology"], "users"=>["Atsushi Ugajin", "Taketoshi Kiya", "Takekazu Kunieda", "Masato Ono", "Tadaharu Yoshida", "Takeo Kubo"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0032902.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sampling_of_workers_from_an_artificially_formed_hot_defensive_bee_ball_/338085", "title"=>"Sampling of workers from an artificially formed hot defensive bee ball.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-14 02:14:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/667730"], "description"=>"<p>(A) Schematic diagram of the lateral view of a bee brain. The green line indicates the position of sections that correspond to a middle part of the brain used for this <i>in situ</i> hybridization experiment. (B) Schematic representation of the <i>Acks</i> signals detected in the right brain hemisphere of the workers that formed the bee ball. The red dots indicate induced <i>Acks</i> signals at 30 or 60 min after the bee ball formation. The boxed regions (a–e) correspond to the Class I KCs whose somata are located inside the calyces (a), parts of the Class II KCs whose somata are located outside of calyces (b and c), the restricted area located between the DL and lobula of the OL (d), and a part of the OL (e), whose <i>in situ</i> hybridization results are presented in the right panels (D–R). (C) Magnified schematic representation of the MB indicating the distribution of the somata of the Class I (green) and the Class II KCs (yellow), respectively. (D–R) <i>In situ</i> hybridization of <i>Acks</i> in each brain area shown in (B) in the brains of workers at 0 (D, G, J, M, and P), 30 (E, H, K, N, and Q) and 60 min (F, I, L, O, and R) after the bee ball formation. (D–F), (G–I), (J–L), (M–O), and (P–R) correspond to the boxed brain regions (a), (b), (c), (d), and (e), respectively. The dotted <i>Acks</i> signals were detected most densely in the Class II KCs (H, I, K, and L), and less densely in the Class I KCs (E and F) at 30 and 60 min after the bee ball formation, respectively. Note that the <i>Acks</i> signals were detected moderately in the restricted region between the DLs and the lobula of the OLs (O), and less densely in the OLs (R) at 60 min after the bee ball formation. Staining observed in area surrounded by dotted ellipse (P–R) represents non-specific staining of trachea, which was also observed in sections hybridized with the sense probe (data not shown). Bars indicate 50 µm. (S) Quantification of <i>Acks</i>-positive cells in various brain regions. Values are means ± SEM. Asterisks indicate significant difference compared to that at 0 min (*, <i>P</i><0.05; **, <i>P</i><0.01; Dunnett's test).</p>", "links"=>[], "tags"=>["neuroscience", "Evolutionary biology"], "article_id"=>338216, "categories"=>["Neuroscience", "Evolutionary Biology"], "users"=>["Atsushi Ugajin", "Taketoshi Kiya", "Takekazu Kunieda", "Masato Ono", "Tadaharu Yoshida", "Takeo Kubo"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0032902.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Neural_activity_in_the_middle_part_of_the_brain_during_bee_ball_formation_/338216", "title"=>"Neural activity in the middle part of the brain during bee ball formation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-14 02:16:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/667890"], "description"=>"<p>(A–L) <i>In situ</i> hybridization of <i>Acks</i> in each brain area shown as <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0032902#pone-0032902-g004\" target=\"_blank\">Figure 4B</a> in the brains of workers exposed to 46°C heat (A, D, G, and J), workers whose antennae are deprived before heat-exposure (B, E, H, and K), and workers exposed to IAA (C, F, I, and L). (A–C), (D–F), (G–I), and (J–L) correspond to the boxed brain regions shown as in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0032902#pone-0032902-g004\" target=\"_blank\">Figure 4B</a> (a), (b), (c), and (d), respectively. In the brains of heat-exposed bees, the dotted <i>Acks</i> signals were detected most densely in the Class II KCs (D and G) and moderately in the restricted area between the DLs and OLs (J), and much less densely in the Class I KCs (A), whereas there was some decrease in the <i>Acks</i> signals in the Class II KCs of antennae-deprived and heat-exposed workers (E and H). On the other hand, scarce or no significant signals were detected in these brain regions in IAA-exposed workers (C, F, I, and L). Bars indicate 50 µm. (M) Quantification of <i>Acks</i>-positive cells in various brain regions. Values are means ± SEM. Asterisks indicate significant difference compared to control (*, <i>P</i><0.05; **, <i>P</i><0.01; Dunnett's test). Student's <i>t</i>-test was used to compare heat-exposed intact and heat-exposed antennae-deprived workers (n.s. = non-significant; **, <i>P</i><0.01). (N) The results of quantitative RT-PCR showing the <i>Acks</i> expression in the MBs of intact and antennae-deprived workers under usual (33°C) and high (46°C) temperature. Each experimental group contained four lots of workers. A two-way ANOVA revealed that there was no interaction between temperature and ablation of antennae (n.s. = non-significant, <i>P</i> = 0.15), and then Student's <i>t</i>-test was conducted for intergroup comparison (**, <i>P</i><0.01). Values are means ± SEM. (O) The results of quantitative RT-PCR showing <i>Acks</i> expression in the brain, thorax, and abdomen of heat-exposed intact workers. Asterisks indicate a significant difference between heat-exposed and control workers within the same tissues (**, <i>P</i><0.01; Student's <i>t</i>-test). The results for the thorax and abdomen are shown in the magnified graph because these values were extremely low. Values are means ± SEM.</p>", "links"=>[], "tags"=>["brains", "workers", "exposed"], "article_id"=>338378, "categories"=>["Neuroscience", "Evolutionary Biology"], "users"=>["Atsushi Ugajin", "Taketoshi Kiya", "Takekazu Kunieda", "Masato Ono", "Tadaharu Yoshida", "Takeo Kubo"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0032902.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Neural_activity_in_the_brains_of_workers_exposed_to_high_temperature_or_IAA_/338378", "title"=>"Neural activity in the brains of workers exposed to high temperature or IAA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-14 02:19:38"}

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Relative Metric

{"start_date"=>"2012-01-01T00:00:00Z", "end_date"=>"2012-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[322, 550, 671, 773, 864, 955, 1048, 1135, 1223, 1308, 1387, 1465, 1534, 1602, 1673, 1744, 1813, 1885, 1955, 2026, 2093, 2160, 2228, 2290, 2349]}, {"subject_area"=>"/Biology and life sciences/Biochemistry", "average_usage"=>[316, 541, 663, 766, 856, 950, 1041, 1128, 1218, 1302, 1382, 1456, 1526, 1593, 1657, 1729, 1796, 1862, 1930, 1999, 2065, 2132, 2202, 2261, 2319]}, {"subject_area"=>"/Biology and life sciences/Computational biology", "average_usage"=>[375, 629, 760, 889, 1000, 1110, 1203, 1298, 1399, 1492, 1603, 1699, 1774, 1855, 1918, 1998, 2062, 2152, 2227, 2312, 2378, 2461, 2528, 2600, 2664]}, {"subject_area"=>"/Biology and life sciences/Organisms", "average_usage"=>[331, 557, 677, 777, 868, 960, 1050, 1136, 1223, 1307, 1390, 1466, 1536, 1603, 1673, 1741, 1814, 1889, 1954, 2028, 2096, 2164, 2233, 2305, 2362]}, {"subject_area"=>"/Medicine and health sciences/Neurology", "average_usage"=>[337, 591, 725, 836, 937, 1024, 1130, 1228, 1320, 1410, 1494, 1571, 1648, 1717, 1796, 1868, 1938, 2007, 2086, 2154, 2221, 2297, 2349, 2411, 2484]}]}
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