We are pleased to introduce the collection Individual and Social Behaviors - Editor’s Pick 2022. This collection showcases most well-received spontaneous articles from the past couple of years, and have been specially handpicked by our Specialty Chief Editor, Prof. Walter Adriani. The work presented here highlights the broad diversity of research performed across the journal, and aims to put a spotlight on the main areas of interest. All research presented here displays strong advances in theory, experiment and methodology with applications to compelling problems. This collection aims to further support Frontiers’ strong community by recognizing highly deserving authors.

National Institute of Health (ISS)

Explore cutting-edge contributions from Walter Adriani and other leading authors across multiple fields of research.

. This research topic focuses on the effects of various biological and neurological factors on behavior. Specifically, it looks at the roles of the medial prefrontal cortex, zona incerta, ventromedial prefrontal cortex, right dorsolateral prefrontal cortex, vomeronasal organ, and action factor in influencing social cognition, cooperative behavior, maximization tendencies, sexual differentiation of behavior, and moral judgment. <ul> <li>Mice with 6-OHDA-induced medial prefrontal cortical (mPFC) injury were found to be more sensitive to social defeat stress and have more significant social cognitive impairment than the control group.</li> <li>Silencing Zona incerta (ZI) significantly blocked the expression of RSDS-induced social CPA and altered PTSD-associated behaviors.</li> <li>The ventromedial prefrontal cortex (VMPFC) was found to play a causal role in cooperative behavior concerning gains and losses.</li> <li>Noninvasive interventions on the right dorsolateral prefrontal cortex were found to increase maximization tendencies, driven by motivational changes rather than working memory improvement.</li> <li>Ablation of the vomeronasal organ (VNO) during either the peripubertal period or adulthood alters socio-sexual behavior in mice, but does not affect sex-typical copulatory behaviors.</li> <li>People were found to have a strong omission bias when it comes to moral judgment, and the action factor was found to modulate the conscious reasoning process during moral judgment.</li> </ul>

Views

Article Views

Article Downloads

Frontiers in Behavioral Neuroscience

Individual and Social Behaviors

Individual and Social Behaviors - Editor’s Pick 2022

Background: Social stress factors in schizophrenia have long-term effects, but will only induce symptoms in a portion of individuals, even if exposed to identical stress.Methods: In the current experiment, we examined mice with 6-hydroxydopamine (6-OHDA)-induced medial prefrontal cortical (mPFC) injury to select for members of a “stress-susceptible group,” and observed the changes in their behavior and the expression of D1 and D2 dopamine receptors in the amygdala and hippocampus.Results: We observed that after chronic social defeat stress, 72.6% of the 6-OHDA lesioned mice exhibited stress response to aggressors, compared to 52.3% of the blank control group. Both the 6-OHDA lesion + social defeat and social defeat groups exhibited anxiety and depression-like behavior. However, social cognitive impairment in the mice from the 6-OHDA lesion + social defeat group was more significant and the D1 expression levels in the amygdala were significantly decreased.Conclusion: These results suggest that the reason that adolescent mice with cortical injury were highly sensitive to defeat stress and had more prominent social cognitive impairment may be the decreased selectivity of D1 in the amygdala.

Background: Social stress factors in schizophrenia have long-term effects, but will only induce symptoms in a portion of individuals, even if exposed to identical stress.Methods: In the current experiment, we examined mice with 6-hydroxydopamine (6-OHDA)-induced medial prefrontal cortical (mPFC) injury to select for members of a “stress-susceptible group,” and observed the changes in their behavior and the expression of D1 and D2 dopamine receptors in the amygdala and hippocampus.Results: We observed that after chronic social defeat stress, 72.6% of the 6-OHDA lesioned mice exhibited stress response to aggressors, compared to 52.3% of the blank control group. Both the 6-OHDA lesion + social defeat and social defeat groups exhibited anxiety and depression-like behavior. However, social cognitive impairment in the mice from the 6-OHDA lesion + social defeat group was more significant and the D1 expression levels in the amygdala were significantly decreased.Conclusion: These results suggest that the reason that adolescent mice with cortical injury were highly sensitive to defeat stress and had more prominent social cognitive impairment may be the decreased selectivity of D1 in the amygdala.

Effects of Chronic Social Defeat Stress on Behavior and Dopamine Receptors in Adolescent Mice With 6-Hydroxydopamine Lesions of the Medial Prefrontal Cortex

Zona incerta (ZI), a largely inhibitory subthalamic region connected with many brain areas, has been suggested to serve as an integrative node for modulation of behaviors and physiological states, such as fear memory conditioning and aversion responses. It is, however, unclear whether ZI regulated the repeated social defeat stress (RSDS)-induced social conditioned place aversion (CPA) and post-traumatic stress disorder (PTSD)-like behaviors. In this study, the function of ZI was silenced via bilateral injection of tetanus toxin light chain (Tet-tox), a neurotoxin that completely blocks the evoked synaptic transmissions, expressing adeno-associated viruses (AAVs). We found ZI silencing: (1) significantly blocked the expression of RSDS-induced social CPA with no effect on the innate preference; (2) significantly enhanced the anxiety level in mice experienced RSDS with no effect on the locomotion activity; (3) altered the PTSD-associated behaviors, including the promotion of spatial cognitive impairment and the preventions of PPI deficit and social avoidance behavior. These effects were not observed on non-stressed mice. In summary, our results suggest the important role of ZI in modulating RSDS-induced social CPA and PTSD-like behaviors.

Zona incerta (ZI), a largely inhibitory subthalamic region connected with many brain areas, has been suggested to serve as an integrative node for modulation of behaviors and physiological states, such as fear memory conditioning and aversion responses. It is, however, unclear whether ZI regulated the repeated social defeat stress (RSDS)-induced social conditioned place aversion (CPA) and post-traumatic stress disorder (PTSD)-like behaviors. In this study, the function of ZI was silenced via bilateral injection of tetanus toxin light chain (Tet-tox), a neurotoxin that completely blocks the evoked synaptic transmissions, expressing adeno-associated viruses (AAVs). We found ZI silencing: (1) significantly blocked the expression of RSDS-induced social CPA with no effect on the innate preference; (2) significantly enhanced the anxiety level in mice experienced RSDS with no effect on the locomotion activity; (3) altered the PTSD-associated behaviors, including the promotion of spatial cognitive impairment and the preventions of PPI deficit and social avoidance behavior. These effects were not observed on non-stressed mice. In summary, our results suggest the important role of ZI in modulating RSDS-induced social CPA and PTSD-like behaviors.

Inactivation of Zona Incerta Blocks Social Conditioned Place Aversion and Modulates Post-traumatic Stress Disorder-Like Behaviors in Mice

Although humans constitute an exceptionally cooperative species that is able to collaborate on large scales for common benefits, cooperation remains a longstanding puzzle in biological and social science. Moreover, cooperation is not always related to resource allocation and gains but is often related to losses. Revealing the neurological mechanisms and brain regions related to cooperation is important for reinforcing cooperation-related gains and losses. Recent neuroscience studies have found that the decision-making process of cooperation is involved in the function of the ventromedial prefrontal cortex (VMPFC). In the present study, we aimed to investigate the causal role of the VMPFC in cooperative behavior concerning gains and losses through the application of transcranial direct current stimulation (tDCS). We integrated cooperation-related gains and losses into a unified paradigm. Based on the paradigm, we researched cooperation behaviors regarding gains in standard public good games and introduced public bad games to investigate cooperative behavior regarding losses. Our study revealed that the VMPFC plays different roles concerning gains and losses in situations requiring cooperation. Anodal stimulation over the VMPFC decreased cooperative behavior in public bad games, whereas stimulation over the VMPFC did not change cooperative behavior in public good games. Moreover, participants’ beliefs about others’ cooperation were changed in public bad games but not in public good games. Finally, participants’ cooperative attitudes were not influenced in the public good or public bad games under the three stimulation conditions.

Although humans constitute an exceptionally cooperative species that is able to collaborate on large scales for common benefits, cooperation remains a longstanding puzzle in biological and social science. Moreover, cooperation is not always related to resource allocation and gains but is often related to losses. Revealing the neurological mechanisms and brain regions related to cooperation is important for reinforcing cooperation-related gains and losses. Recent neuroscience studies have found that the decision-making process of cooperation is involved in the function of the ventromedial prefrontal cortex (VMPFC). In the present study, we aimed to investigate the causal role of the VMPFC in cooperative behavior concerning gains and losses through the application of transcranial direct current stimulation (tDCS). We integrated cooperation-related gains and losses into a unified paradigm. Based on the paradigm, we researched cooperation behaviors regarding gains in standard public good games and introduced public bad games to investigate cooperative behavior regarding losses. Our study revealed that the VMPFC plays different roles concerning gains and losses in situations requiring cooperation. Anodal stimulation over the VMPFC decreased cooperative behavior in public bad games, whereas stimulation over the VMPFC did not change cooperative behavior in public good games. Moreover, participants&#x2019; beliefs about others&#x2019; cooperation were changed in public bad games but not in public good games. Finally, participants&#x2019; cooperative attitudes were not influenced in the public good or public bad games under the three stimulation conditions.

The Role of the Ventromedial Prefrontal Cortex in Public Good and Public Bad Games: Evidence From a tDCS Study

People seek the best in every aspect of life. However, little is known about the neurobiological mechanisms supporting this process of maximization. In this study, maximization tendencies were increased by using high-definition transcranial direct current stimulation (HD-tDCS) over the right dorsolateral prefrontal cortex (DLPFC). Participants (n = 64) received 2 mA anodal 4 × 1 HD-tDCS or sham stimulation over the right DLPFC in two sessions and subsequently completed an N-back working memory task and a maximization scale (MS). We observed that maximization tendency scores increased during anodal stimulation. Furthermore, the results indicate that this increase in maximization tendency was driven by motivational changes. On the MS, alternative search subscale scores were significantly increased, demonstrating an increase in motivation to evaluate more alternatives; however, the results did not indicate that the increase in maximization tendencies was due to working memory improvement. These results demonstrated that maximization tendencies can be strengthened through noninvasive interventions and that the right DLPFC has a causal relationship with maximization tendencies.

People seek the best in every aspect of life. However, little is known about the neurobiological mechanisms supporting this process of maximization. In this study, maximization tendencies were increased by using high-definition transcranial direct current stimulation (HD-tDCS) over the right dorsolateral prefrontal cortex (DLPFC). Participants (n = 64) received 2 mA anodal 4 × 1 HD-tDCS or sham stimulation over the right DLPFC in two sessions and subsequently completed an N-back working memory task and a maximization scale (MS). We observed that maximization tendency scores increased during anodal stimulation. Furthermore, the results indicate that this increase in maximization tendency was driven by motivational changes. On the MS, alternative search subscale scores were significantly increased, demonstrating an increase in motivation to evaluate more alternatives; however, the results did not indicate that the increase in maximization tendencies was due to working memory improvement. These results demonstrated that maximization tendencies can be strengthened through noninvasive interventions and that the right DLPFC has a causal relationship with maximization tendencies.

High-Definition Transcranial Direct Current Stimulation Over the Right Lateral Prefrontal Cortex Increases Maximization Tendencies

Genetic disruption of the vomeronasal organ (VNO), an organ responsible for pheromone processing, drastically alters socio-sexual behavior in mice. However, it is not known whether the VNO has a role during the pubertal organizational period when sex-typical socio-sexual behaviors emerge, or if disruption of the organ in adulthood is sufficient to alter socio-sexual behavior. To bypass the lifelong VNO disruption of genetic knockout models, we surgically ablated the VNO of male and female mice either during the peripubertal period [postnatal day (PND) 28–30] or adulthood (PND 58–60), with sham controls at both ages. We ruled out anosmia via the buried food test and assessed sexual odor preferences by simultaneously exposing mice to same- and opposite-sex soiled-bedding. We then measured territorial aggression with the resident-intruder paradigm and assessed sexual behavior in response to an encounter with an estrus-induced female. Neural activity approximated by FOS-immunoreactivity along the VNO-accessory olfactory pathway was measured in response to opposite-sex odors. We found that peripubertal VNO ablation decreased sexual odor preferences and neural activity in response to opposite-sex odors, and drastically reduced territorial aggression in male mice. Conversely, adult VNO ablation resulted in subtle differences in sexual odor preferences compared with sham controls. Regardless of the VNO condition, mice displayed sex-typical copulatory behaviors. Together, these results suggest that puberty is a critical period in development whereby the VNO contributes to the sexual differentiation of behavior and neural response to conspecific odors.

Genetic disruption of the vomeronasal organ (VNO), an organ responsible for pheromone processing, drastically alters socio-sexual behavior in mice. However, it is not known whether the VNO has a role during the pubertal organizational period when sex-typical socio-sexual behaviors emerge, or if disruption of the organ in adulthood is sufficient to alter socio-sexual behavior. To bypass the lifelong VNO disruption of genetic knockout models, we surgically ablated the VNO of male and female mice either during the peripubertal period [postnatal day (PND) 28–30] or adulthood (PND 58–60), with sham controls at both ages. We ruled out anosmia via the buried food test and assessed sexual odor preferences by simultaneously exposing mice to same- and opposite-sex soiled-bedding. We then measured territorial aggression with the resident-intruder paradigm and assessed sexual behavior in response to an encounter with an estrus-induced female. Neural activity approximated by FOS-immunoreactivity along the VNO-accessory olfactory pathway was measured in response to opposite-sex odors. We found that peripubertal VNO ablation decreased sexual odor preferences and neural activity in response to opposite-sex odors, and drastically reduced territorial aggression in male mice. Conversely, adult VNO ablation resulted in subtle differences in sexual odor preferences compared with sham controls. Regardless of the VNO condition, mice displayed sex-typical copulatory behaviors. Together, these results suggest that puberty is a critical period in development whereby the VNO contributes to the sexual differentiation of behavior and neural response to conspecific odors.

Puberty is a Critical Period for Vomeronasal Organ Mediation of Socio-sexual Behavior in Mice

Moral judgment can be highly affected by the action and intention factors on a behavior level. Previous neuroimaging studies have demonstrated that the intention factor can modulate both the affective and cognitive processing of moral judgment. The present event-related potentials (ERP) study examined how the action factor modulated the neural dynamics of moral judgment under a newly developed moral dilemma paradigm including three different conditions: harm caused by action (i.e., doing harm), harm caused by omission (i.e., allowing harm), and no harm. Behavior data showed that participants preferred utilitarian judgments and spent less time on the allowing harm condition than for the doing harm condition. ERP results revealed that, compared with the doing harm and no harm dilemmas, the allowing harm dilemmas elicited an enhanced N450 response associated with cognitive control and/or cognitive effort processes, but attenuated a late positive potentials (LPP) response associated with top-down control of attention and cognitive “rational” control processes. Such LPP amplitude differences were positively correlated with the C-score of the moral competence test which indexed the cognitive aspect of moral judgment competency. These findings suggested that people have a strong omission bias, and such an action factor modulates the conscious reasoning process during moral judgment, including the cognitive control and/or cognitive effort, and attentional allocation processes.

Moral judgment can be highly affected by the action and intention factors on a behavior level. Previous neuroimaging studies have demonstrated that the intention factor can modulate both the affective and cognitive processing of moral judgment. The present event-related potentials (ERP) study examined how the action factor modulated the neural dynamics of moral judgment under a newly developed moral dilemma paradigm including three different conditions: harm caused by action (i.e., doing harm), harm caused by omission (i.e., allowing harm), and no harm. Behavior data showed that participants preferred utilitarian judgments and spent less time on the allowing harm condition than for the doing harm condition. ERP results revealed that, compared with the doing harm and no harm dilemmas, the allowing harm dilemmas elicited an enhanced N450 response associated with cognitive control and/or cognitive effort processes, but attenuated a late positive potentials (LPP) response associated with top-down control of attention and cognitive &#x201c;rational&#x201d; control processes. Such LPP amplitude differences were positively correlated with the C-score of the moral competence test which indexed the cognitive aspect of moral judgment competency. These findings suggested that people have a strong omission bias, and such an action factor modulates the conscious reasoning process during moral judgment, including the cognitive control and/or cognitive effort, and attentional allocation processes.