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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Veröffentlicht in:Pesticide biochemistry and physiology 2024-11, Vol.205, p.106167, Article 106167
Hauptverfasser: 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
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container_start_page 106167
container_title Pesticide biochemistry and physiology
container_volume 205
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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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><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. 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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 ; 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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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