Adolescent Social Stress Increases Anxiety-like Behavior and Alters Synaptic Transmission, Without Influencing Nicotine Responses, in a Sex-Dependent Manner

Michael J. Caruso, Nicole Crowley, Dana E. Reiss, Jasmine I. Caulfield, Bernhard Luscher, Sonia Angele Cavigelli, Helen Marie Kamens

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Abstract

Early-life stress is a risk factor for comorbid anxiety and nicotine use. Because little is known about the factors underlying this comorbidity, we investigated the effects of adolescent stress on anxiety-like behavior and nicotine responses within individual animals. Adolescent male and female C57BL/6J mice were exposed to chronic variable social stress (CVSS; repeated cycles of social isolation + social reorganization) or control conditions from postnatal days (PND) 25–59. Anxiety-like behavior and social avoidance were measured in the elevated plus-maze (PND 61–65) and social approach-avoidance test (Experiment 1: PND 140–144; Experiment 2: 95–97), respectively. Acute nicotine-induced locomotor, hypothermic, corticosterone responses, (Experiment 1: PND 56–59; Experiment 2: PND 65–70) and voluntary oral nicotine consumption (Experiment 1: PND 116–135; Experiment 2: 73–92) were also examined. Finally, we assessed prefrontal cortex (PFC) and nucleus accumbens (NAC) synaptic transmission (PND 64–80); brain regions that are implicated in anxiety and addiction. Mice exposed to adolescent CVSS displayed increased anxiety-like behavior relative to controls. Further, CVSS altered synaptic excitability in PFC and NAC neurons in a sex-specific manner. For males, CVSS decreased the amplitude and frequency of spontaneous excitatory postsynaptic currents in the PFC and NAC, respectively. In females, CVSS decreased the amplitude of spontaneous inhibitory postsynaptic currents in the NAC. Adolescent CVSS did not affect social avoidance or nicotine responses and anxiety-like behavior was not reliably associated with nicotine responses within individual animals. Taken together, complex interactions between PFC and NAC function may contribute to adolescent stress-induced anxiety-like behavior without influencing nicotine responses.

Original languageEnglish (US)
Pages (from-to)182-198
Number of pages17
JournalNeuroscience
Volume373
DOIs
StatePublished - Mar 1 2018

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Nicotine
Synaptic Transmission
Nucleus Accumbens
Anxiety
Prefrontal Cortex
Avoidance Learning
Inhibitory Postsynaptic Potentials
Social Isolation
Excitatory Postsynaptic Potentials
Corticosterone
Inbred C57BL Mouse
Psychological Stress
Comorbidity
Neurons
Brain

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)

Cite this

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title = "Adolescent Social Stress Increases Anxiety-like Behavior and Alters Synaptic Transmission, Without Influencing Nicotine Responses, in a Sex-Dependent Manner",
abstract = "Early-life stress is a risk factor for comorbid anxiety and nicotine use. Because little is known about the factors underlying this comorbidity, we investigated the effects of adolescent stress on anxiety-like behavior and nicotine responses within individual animals. Adolescent male and female C57BL/6J mice were exposed to chronic variable social stress (CVSS; repeated cycles of social isolation + social reorganization) or control conditions from postnatal days (PND) 25–59. Anxiety-like behavior and social avoidance were measured in the elevated plus-maze (PND 61–65) and social approach-avoidance test (Experiment 1: PND 140–144; Experiment 2: 95–97), respectively. Acute nicotine-induced locomotor, hypothermic, corticosterone responses, (Experiment 1: PND 56–59; Experiment 2: PND 65–70) and voluntary oral nicotine consumption (Experiment 1: PND 116–135; Experiment 2: 73–92) were also examined. Finally, we assessed prefrontal cortex (PFC) and nucleus accumbens (NAC) synaptic transmission (PND 64–80); brain regions that are implicated in anxiety and addiction. Mice exposed to adolescent CVSS displayed increased anxiety-like behavior relative to controls. Further, CVSS altered synaptic excitability in PFC and NAC neurons in a sex-specific manner. For males, CVSS decreased the amplitude and frequency of spontaneous excitatory postsynaptic currents in the PFC and NAC, respectively. In females, CVSS decreased the amplitude of spontaneous inhibitory postsynaptic currents in the NAC. Adolescent CVSS did not affect social avoidance or nicotine responses and anxiety-like behavior was not reliably associated with nicotine responses within individual animals. Taken together, complex interactions between PFC and NAC function may contribute to adolescent stress-induced anxiety-like behavior without influencing nicotine responses.",
author = "Caruso, {Michael J.} and Nicole Crowley and Reiss, {Dana E.} and Caulfield, {Jasmine I.} and Bernhard Luscher and Cavigelli, {Sonia Angele} and Kamens, {Helen Marie}",
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AU - Caruso, Michael J.

AU - Crowley, Nicole

AU - Reiss, Dana E.

AU - Caulfield, Jasmine I.

AU - Luscher, Bernhard

AU - Cavigelli, Sonia Angele

AU - Kamens, Helen Marie

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N2 - Early-life stress is a risk factor for comorbid anxiety and nicotine use. Because little is known about the factors underlying this comorbidity, we investigated the effects of adolescent stress on anxiety-like behavior and nicotine responses within individual animals. Adolescent male and female C57BL/6J mice were exposed to chronic variable social stress (CVSS; repeated cycles of social isolation + social reorganization) or control conditions from postnatal days (PND) 25–59. Anxiety-like behavior and social avoidance were measured in the elevated plus-maze (PND 61–65) and social approach-avoidance test (Experiment 1: PND 140–144; Experiment 2: 95–97), respectively. Acute nicotine-induced locomotor, hypothermic, corticosterone responses, (Experiment 1: PND 56–59; Experiment 2: PND 65–70) and voluntary oral nicotine consumption (Experiment 1: PND 116–135; Experiment 2: 73–92) were also examined. Finally, we assessed prefrontal cortex (PFC) and nucleus accumbens (NAC) synaptic transmission (PND 64–80); brain regions that are implicated in anxiety and addiction. Mice exposed to adolescent CVSS displayed increased anxiety-like behavior relative to controls. Further, CVSS altered synaptic excitability in PFC and NAC neurons in a sex-specific manner. For males, CVSS decreased the amplitude and frequency of spontaneous excitatory postsynaptic currents in the PFC and NAC, respectively. In females, CVSS decreased the amplitude of spontaneous inhibitory postsynaptic currents in the NAC. Adolescent CVSS did not affect social avoidance or nicotine responses and anxiety-like behavior was not reliably associated with nicotine responses within individual animals. Taken together, complex interactions between PFC and NAC function may contribute to adolescent stress-induced anxiety-like behavior without influencing nicotine responses.

AB - Early-life stress is a risk factor for comorbid anxiety and nicotine use. Because little is known about the factors underlying this comorbidity, we investigated the effects of adolescent stress on anxiety-like behavior and nicotine responses within individual animals. Adolescent male and female C57BL/6J mice were exposed to chronic variable social stress (CVSS; repeated cycles of social isolation + social reorganization) or control conditions from postnatal days (PND) 25–59. Anxiety-like behavior and social avoidance were measured in the elevated plus-maze (PND 61–65) and social approach-avoidance test (Experiment 1: PND 140–144; Experiment 2: 95–97), respectively. Acute nicotine-induced locomotor, hypothermic, corticosterone responses, (Experiment 1: PND 56–59; Experiment 2: PND 65–70) and voluntary oral nicotine consumption (Experiment 1: PND 116–135; Experiment 2: 73–92) were also examined. Finally, we assessed prefrontal cortex (PFC) and nucleus accumbens (NAC) synaptic transmission (PND 64–80); brain regions that are implicated in anxiety and addiction. Mice exposed to adolescent CVSS displayed increased anxiety-like behavior relative to controls. Further, CVSS altered synaptic excitability in PFC and NAC neurons in a sex-specific manner. For males, CVSS decreased the amplitude and frequency of spontaneous excitatory postsynaptic currents in the PFC and NAC, respectively. In females, CVSS decreased the amplitude of spontaneous inhibitory postsynaptic currents in the NAC. Adolescent CVSS did not affect social avoidance or nicotine responses and anxiety-like behavior was not reliably associated with nicotine responses within individual animals. Taken together, complex interactions between PFC and NAC function may contribute to adolescent stress-induced anxiety-like behavior without influencing nicotine responses.

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