Disruption of exploratory behavior and olfactory memory in cockroaches exposed to sublethal doses of the neonicotinoid Thiamethoxam
Neonicotinoid insecticides (NNI) are agonists of insect nicotinic acetylcholine receptors (nAChR) that induce non-elucidate mechanisms of abnormal behavior in insects. In this work, we investigated the effects of sublethal doses of the neonicotinoid thiamethoxam (TMX) on neurochemical and physiologi...
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creator | Ferreira, Letícia Campos Rosa, Maria Eduarda Rodrigues, Luis Guilherme Silva Dias, Diego Roberto Colombo de Paiva Guimarães, Marcelo Valsecchi, Chiara Queiroz de Souza, Velci de Faria Barbosa, Renata Vinadé, Lucia Helena Hyslop, Stephen da Rocha, João Batista Teixeira Dal Belo, Cháriston André |
description | Neonicotinoid insecticides (NNI) are agonists of insect nicotinic acetylcholine receptors (nAChR) that induce non-elucidate mechanisms of abnormal behavior in insects. In this work, we investigated the effects of sublethal doses of the neonicotinoid thiamethoxam (TMX) on neurochemical and physiological parameters in cockroaches. Sublethal doses of TMX (0.01–10 ng.g−1 body mass) caused significant alterations in most of the neurophysiological parameters evaluated. TMX reduced sustained locomotor activity by 19.9–25.8 %, depending on the dose. Leg grooming activity increased by 124.5 ± 3.4 %, 158.7 ± 3.5 %, 168.3 ± 3.4 %, and 160.4 ± 3.4 % (mean ± SEM) with TMX doses of 0.01, 0.1, 1, and 10 ng.g−1, respectively. Exploratory activity was significantly reduced only at the lowest TMX dose (0.01 ng.g−1) – the time spent immobile increased from 30 % to ∼45 %, whereas none of the doses affected the walking speed. Treatment with TMX (0.01 ng.g−1) markedly reduced the olfactory sensitivity of the cockroaches and also reduced the mechanosensory action potential amplitude, rise time and decay time by 61.2 ± 19 %, 50 ± 4 %, and 76.8 ± 9.5 %, respectively. In semi-isolated heart preparations, TMX caused positive chronotropism (increases of 34.7 ± 15.9 %, 26.8 ± 7.8 %, 43.0 ± 16.5 %, and 19.0 ± 13.7 % for 0.01, 0.1, 1, and 10 ng of TMX, respectively). TMX attenuated the activity of glutathione-S-transferase by 35.1 ± 6.4 % at the highest dose tested (10 ng.g−1). TMX caused alterations in the metal ion content of cockroach brains that varied with the dose tested and the ion examined. These findings indicate that sublethal doses of TMX can interfere with normal neurological function in cockroaches and disrupt brain metal ion homeostasis.
[Display omitted]
•Thiamethoxam is an agonist of insect nicotinic acetylcholine receptors (nAChR).•Thiamethoxam disrupt the somatosensorial integration in insects.•Thiamethoxam induces functional alterations of insect brain metal ion homeostasis.•These actions adversely affect neuronal pathways involved in insect behavior. |
doi_str_mv | 10.1016/j.pestbp.2024.106167 |
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[Display omitted]
•Thiamethoxam is an agonist of insect nicotinic acetylcholine receptors (nAChR).•Thiamethoxam disrupt the somatosensorial integration in insects.•Thiamethoxam induces functional alterations of insect brain metal ion homeostasis.•These actions adversely affect neuronal pathways involved in insect behavior.</description><identifier>ISSN: 0048-3575</identifier><identifier>ISSN: 1095-9939</identifier><identifier>EISSN: 1095-9939</identifier><identifier>DOI: 10.1016/j.pestbp.2024.106167</identifier><identifier>PMID: 39477619</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>abnormal behavior ; acetylcholine ; action potentials ; Animals ; Behavior, Animal - drug effects ; Blattodea ; body weight ; brain ; Cockroaches - drug effects ; Dose-Response Relationship, Drug ; Entomotoxicity ; Exploratory Behavior - drug effects ; glutathione transferase ; heart ; homeostasis ; Insecticides - toxicity ; insects ; locomotion ; Male ; memory ; Memory - drug effects ; Neonicotinoids ; Neonicotinoids - toxicity ; neurophysiology ; Nitro Compounds - toxicity ; Oxazines - toxicity ; Smell - drug effects ; Somatosensation ; Sublethal effects ; thiamethoxam ; Thiamethoxam - toxicity ; Thiazoles - toxicity ; Trace metals</subject><ispartof>Pesticide biochemistry and physiology, 2024-11, Vol.205, p.106167, Article 106167</ispartof><rights>2024 Elsevier Inc.</rights><rights>Copyright © 2024 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c274t-d0dfc56ac59c8f4611f41d08a884dc347641c5b609d535613b7fda46c85be76a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0048357524004000$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39477619$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ferreira, Letícia Campos</creatorcontrib><creatorcontrib>Rosa, Maria Eduarda</creatorcontrib><creatorcontrib>Rodrigues, Luis Guilherme Silva</creatorcontrib><creatorcontrib>Dias, Diego Roberto Colombo</creatorcontrib><creatorcontrib>de Paiva Guimarães, Marcelo</creatorcontrib><creatorcontrib>Valsecchi, Chiara</creatorcontrib><creatorcontrib>Queiroz de Souza, Velci</creatorcontrib><creatorcontrib>de Faria Barbosa, Renata</creatorcontrib><creatorcontrib>Vinadé, Lucia Helena</creatorcontrib><creatorcontrib>Hyslop, Stephen</creatorcontrib><creatorcontrib>da Rocha, João Batista Teixeira</creatorcontrib><creatorcontrib>Dal Belo, Cháriston André</creatorcontrib><title>Disruption of exploratory behavior and olfactory memory in cockroaches exposed to sublethal doses of the neonicotinoid Thiamethoxam</title><title>Pesticide biochemistry and physiology</title><addtitle>Pestic Biochem Physiol</addtitle><description>Neonicotinoid insecticides (NNI) are agonists of insect nicotinic acetylcholine receptors (nAChR) that induce non-elucidate mechanisms of abnormal behavior in insects. In this work, we investigated the effects of sublethal doses of the neonicotinoid thiamethoxam (TMX) on neurochemical and physiological parameters in cockroaches. Sublethal doses of TMX (0.01–10 ng.g−1 body mass) caused significant alterations in most of the neurophysiological parameters evaluated. TMX reduced sustained locomotor activity by 19.9–25.8 %, depending on the dose. Leg grooming activity increased by 124.5 ± 3.4 %, 158.7 ± 3.5 %, 168.3 ± 3.4 %, and 160.4 ± 3.4 % (mean ± SEM) with TMX doses of 0.01, 0.1, 1, and 10 ng.g−1, respectively. Exploratory activity was significantly reduced only at the lowest TMX dose (0.01 ng.g−1) – the time spent immobile increased from 30 % to ∼45 %, whereas none of the doses affected the walking speed. Treatment with TMX (0.01 ng.g−1) markedly reduced the olfactory sensitivity of the cockroaches and also reduced the mechanosensory action potential amplitude, rise time and decay time by 61.2 ± 19 %, 50 ± 4 %, and 76.8 ± 9.5 %, respectively. In semi-isolated heart preparations, TMX caused positive chronotropism (increases of 34.7 ± 15.9 %, 26.8 ± 7.8 %, 43.0 ± 16.5 %, and 19.0 ± 13.7 % for 0.01, 0.1, 1, and 10 ng of TMX, respectively). TMX attenuated the activity of glutathione-S-transferase by 35.1 ± 6.4 % at the highest dose tested (10 ng.g−1). TMX caused alterations in the metal ion content of cockroach brains that varied with the dose tested and the ion examined. These findings indicate that sublethal doses of TMX can interfere with normal neurological function in cockroaches and disrupt brain metal ion homeostasis.
[Display omitted]
•Thiamethoxam is an agonist of insect nicotinic acetylcholine receptors (nAChR).•Thiamethoxam disrupt the somatosensorial integration in insects.•Thiamethoxam induces functional alterations of insect brain metal ion homeostasis.•These actions adversely affect neuronal pathways involved in insect behavior.</description><subject>abnormal behavior</subject><subject>acetylcholine</subject><subject>action potentials</subject><subject>Animals</subject><subject>Behavior, Animal - drug effects</subject><subject>Blattodea</subject><subject>body weight</subject><subject>brain</subject><subject>Cockroaches - drug effects</subject><subject>Dose-Response Relationship, Drug</subject><subject>Entomotoxicity</subject><subject>Exploratory Behavior - drug effects</subject><subject>glutathione transferase</subject><subject>heart</subject><subject>homeostasis</subject><subject>Insecticides - toxicity</subject><subject>insects</subject><subject>locomotion</subject><subject>Male</subject><subject>memory</subject><subject>Memory - drug effects</subject><subject>Neonicotinoids</subject><subject>Neonicotinoids - toxicity</subject><subject>neurophysiology</subject><subject>Nitro Compounds - toxicity</subject><subject>Oxazines - toxicity</subject><subject>Smell - drug effects</subject><subject>Somatosensation</subject><subject>Sublethal effects</subject><subject>thiamethoxam</subject><subject>Thiamethoxam - toxicity</subject><subject>Thiazoles - toxicity</subject><subject>Trace metals</subject><issn>0048-3575</issn><issn>1095-9939</issn><issn>1095-9939</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkUtv1TAQhS1ERS8t_wAhL9nkYseveIOEylOq1E27thx7oviSxMFOqnbNH8chhSViNdLRd2ZG5yD0mpIjJVS-Ox1nyEs7H2tS8yJJKtUzdKBEi0prpp-jAyG8qZhQ4hy9zPlECNGc6BfonGmulKT6gH5-DDmt8xLihGOH4WEeYrJLTI-4hd7eh5iwnTyOQ2fdb3mEcRthwi667yla10PejDGDx0vEeW0HWHo7YF-kvK1desATxCm4uIQpBo9v-2DHQsUHO16is84OGV49zQt09_nT7dXX6vrmy7erD9eVqxVfKk9854S0TmjXdFxS2nHqSWObhnvHuJKcOtFKor1gQlLWqs5bLl0jWlDSsgv0dt87p_hjLeGZMWQHw2DLb2s2jArWCEq1-g-0riVTjNCC8h11KeacoDNzCqNNj4YSszVlTmZvymxNmb2pYnvzdGFtR_B_TX-qKcD7HYASyX2AZLILMDnwIYFbjI_h3xd-AZscqYM</recordid><startdate>202411</startdate><enddate>202411</enddate><creator>Ferreira, Letícia Campos</creator><creator>Rosa, Maria Eduarda</creator><creator>Rodrigues, Luis Guilherme Silva</creator><creator>Dias, Diego Roberto Colombo</creator><creator>de Paiva Guimarães, Marcelo</creator><creator>Valsecchi, Chiara</creator><creator>Queiroz de Souza, Velci</creator><creator>de Faria Barbosa, Renata</creator><creator>Vinadé, Lucia Helena</creator><creator>Hyslop, Stephen</creator><creator>da Rocha, João Batista Teixeira</creator><creator>Dal Belo, Cháriston André</creator><general>Elsevier Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope></search><sort><creationdate>202411</creationdate><title>Disruption of exploratory behavior and olfactory memory in cockroaches exposed to sublethal doses of the neonicotinoid Thiamethoxam</title><author>Ferreira, Letícia Campos ; Rosa, Maria Eduarda ; Rodrigues, Luis Guilherme Silva ; Dias, Diego Roberto Colombo ; de Paiva Guimarães, Marcelo ; Valsecchi, Chiara ; Queiroz de Souza, Velci ; de Faria Barbosa, Renata ; Vinadé, Lucia Helena ; Hyslop, Stephen ; da Rocha, João Batista Teixeira ; Dal Belo, Cháriston André</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c274t-d0dfc56ac59c8f4611f41d08a884dc347641c5b609d535613b7fda46c85be76a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>abnormal behavior</topic><topic>acetylcholine</topic><topic>action potentials</topic><topic>Animals</topic><topic>Behavior, Animal - drug effects</topic><topic>Blattodea</topic><topic>body weight</topic><topic>brain</topic><topic>Cockroaches - drug effects</topic><topic>Dose-Response Relationship, Drug</topic><topic>Entomotoxicity</topic><topic>Exploratory Behavior - drug effects</topic><topic>glutathione transferase</topic><topic>heart</topic><topic>homeostasis</topic><topic>Insecticides - toxicity</topic><topic>insects</topic><topic>locomotion</topic><topic>Male</topic><topic>memory</topic><topic>Memory - drug effects</topic><topic>Neonicotinoids</topic><topic>Neonicotinoids - toxicity</topic><topic>neurophysiology</topic><topic>Nitro Compounds - toxicity</topic><topic>Oxazines - toxicity</topic><topic>Smell - drug effects</topic><topic>Somatosensation</topic><topic>Sublethal effects</topic><topic>thiamethoxam</topic><topic>Thiamethoxam - toxicity</topic><topic>Thiazoles - toxicity</topic><topic>Trace metals</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ferreira, Letícia Campos</creatorcontrib><creatorcontrib>Rosa, Maria Eduarda</creatorcontrib><creatorcontrib>Rodrigues, Luis Guilherme Silva</creatorcontrib><creatorcontrib>Dias, Diego Roberto Colombo</creatorcontrib><creatorcontrib>de Paiva Guimarães, Marcelo</creatorcontrib><creatorcontrib>Valsecchi, Chiara</creatorcontrib><creatorcontrib>Queiroz de Souza, Velci</creatorcontrib><creatorcontrib>de Faria Barbosa, Renata</creatorcontrib><creatorcontrib>Vinadé, Lucia Helena</creatorcontrib><creatorcontrib>Hyslop, Stephen</creatorcontrib><creatorcontrib>da Rocha, João Batista Teixeira</creatorcontrib><creatorcontrib>Dal Belo, Cháriston André</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Pesticide biochemistry and physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ferreira, Letícia Campos</au><au>Rosa, Maria Eduarda</au><au>Rodrigues, Luis Guilherme Silva</au><au>Dias, Diego Roberto Colombo</au><au>de Paiva Guimarães, Marcelo</au><au>Valsecchi, Chiara</au><au>Queiroz de Souza, Velci</au><au>de Faria Barbosa, Renata</au><au>Vinadé, Lucia Helena</au><au>Hyslop, Stephen</au><au>da Rocha, João Batista Teixeira</au><au>Dal Belo, Cháriston André</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Disruption of exploratory behavior and olfactory memory in cockroaches exposed to sublethal doses of the neonicotinoid Thiamethoxam</atitle><jtitle>Pesticide biochemistry and physiology</jtitle><addtitle>Pestic Biochem Physiol</addtitle><date>2024-11</date><risdate>2024</risdate><volume>205</volume><spage>106167</spage><pages>106167-</pages><artnum>106167</artnum><issn>0048-3575</issn><issn>1095-9939</issn><eissn>1095-9939</eissn><abstract>Neonicotinoid insecticides (NNI) are agonists of insect nicotinic acetylcholine receptors (nAChR) that induce non-elucidate mechanisms of abnormal behavior in insects. In this work, we investigated the effects of sublethal doses of the neonicotinoid thiamethoxam (TMX) on neurochemical and physiological parameters in cockroaches. Sublethal doses of TMX (0.01–10 ng.g−1 body mass) caused significant alterations in most of the neurophysiological parameters evaluated. TMX reduced sustained locomotor activity by 19.9–25.8 %, depending on the dose. Leg grooming activity increased by 124.5 ± 3.4 %, 158.7 ± 3.5 %, 168.3 ± 3.4 %, and 160.4 ± 3.4 % (mean ± SEM) with TMX doses of 0.01, 0.1, 1, and 10 ng.g−1, respectively. Exploratory activity was significantly reduced only at the lowest TMX dose (0.01 ng.g−1) – the time spent immobile increased from 30 % to ∼45 %, whereas none of the doses affected the walking speed. Treatment with TMX (0.01 ng.g−1) markedly reduced the olfactory sensitivity of the cockroaches and also reduced the mechanosensory action potential amplitude, rise time and decay time by 61.2 ± 19 %, 50 ± 4 %, and 76.8 ± 9.5 %, respectively. In semi-isolated heart preparations, TMX caused positive chronotropism (increases of 34.7 ± 15.9 %, 26.8 ± 7.8 %, 43.0 ± 16.5 %, and 19.0 ± 13.7 % for 0.01, 0.1, 1, and 10 ng of TMX, respectively). TMX attenuated the activity of glutathione-S-transferase by 35.1 ± 6.4 % at the highest dose tested (10 ng.g−1). TMX caused alterations in the metal ion content of cockroach brains that varied with the dose tested and the ion examined. These findings indicate that sublethal doses of TMX can interfere with normal neurological function in cockroaches and disrupt brain metal ion homeostasis.
[Display omitted]
•Thiamethoxam is an agonist of insect nicotinic acetylcholine receptors (nAChR).•Thiamethoxam disrupt the somatosensorial integration in insects.•Thiamethoxam induces functional alterations of insect brain metal ion homeostasis.•These actions adversely affect neuronal pathways involved in insect behavior.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>39477619</pmid><doi>10.1016/j.pestbp.2024.106167</doi></addata></record> |
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subjects | abnormal behavior acetylcholine action potentials Animals Behavior, Animal - drug effects Blattodea body weight brain Cockroaches - drug effects Dose-Response Relationship, Drug Entomotoxicity Exploratory Behavior - drug effects glutathione transferase heart homeostasis Insecticides - toxicity insects locomotion Male memory Memory - drug effects Neonicotinoids Neonicotinoids - toxicity neurophysiology Nitro Compounds - toxicity Oxazines - toxicity Smell - drug effects Somatosensation Sublethal effects thiamethoxam Thiamethoxam - toxicity Thiazoles - toxicity Trace metals |
title | Disruption of exploratory behavior and olfactory memory in cockroaches exposed to sublethal doses of the neonicotinoid Thiamethoxam |
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