Encoding of social exploration by neural ensembles in the insular cortex

Miura, Isamu; Sato, Masaaki; Overton, Eric T. N.; Kunori, Nobuo; Nakai, Junichi; Kawamata, Takakazu; Nakai, Norihiro; Takumi, Toru

doi:10.1371/journal.pbio.3000584

Cited by 27 publications

(34 citation statements)

References 58 publications

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“…While the AI may modulate novel object exploration, its relatively low salience compared to exploration of a conspecific may have drowned out any effects during testing. AI inhibition also had no impact on social interaction with a conspecific in this task, which is antithetical to reports showing inhibition of the insula disrupts social exploration of an unfamiliar animal 44 , while chemogenetic activation of the AI subsequently restored heroin-induced deficits in prosocial behaviors 39 . However, it may corroborate findings in other studies showing the AI may modulate social exploration in a context-dependent manner.…”

Section: Discussionsupporting

confidence: 82%

The role of the anterior insula during targeted helping behavior in male rats

Cox

Kearns

Woods

et al. 2022

Sci Rep

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Empathy, the understanding of the emotional state of others, can be examined across species using the Perception Action Model, where shared affect promotes an action by “Observers” to aid a distressed “Target”. The anterior insula (AI) has garnered interest in empathic behavior due to its role integrating sensory and emotional information of self and other. In the following studies, the AI was inhibited pharmacologically and chemogenetically during targeted helping. We demonstrate the insula is active during, and is necessary for the maintenance of, targeted helping. Analysis of ultrasonic vocalizations revealed distress calls from Targets increased when Observers’ helping was attenuated due to insula inhibition. Targets’ elevated distress was directly correlated to Observers’ diminished helping behavior, suggesting emotional transfer between Observer and Target is blunted following Observer AI inhibition. Finally, the AI may selectively blunt targeted helping, as social exploration did not change in a social reward place conditioning task. These studies help further establish the anterior insula as a critical node in the empathic brain during targeted helping, even in the absence of direct social contact.

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Section: Discussionsupporting

confidence: 82%

The role of the anterior insula during targeted helping behavior in male rats

Cox

Kearns

Woods

et al. 2022

Sci Rep

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“…The foregoing physiological findings suggest that CRF augments synaptic transmission in IC via downregulation of local GABAergic interneurons. Manipulations that alter insular excitability are associated with changes in social affective behaviors [ 29 , 32 , 36 , 37 ] and the CRF system is implicated in many aspects of social behavior [ 15 ]. To begin to assess whether the effect of CRF in the slices was behaviorally relevant, we utilized social interaction behavior tests.…”

Section: Resultsmentioning

confidence: 99%

Insular cortex corticotropin-releasing factor integrates stress signaling with social affective behavior

Rieger

Varela

et al. 2022

Neuropsychopharmacol.

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Impairments in identifying and responding to the emotions of others manifest in a variety of psychopathologies. Therefore, elaborating the neurobiological mechanisms that underpin social responses to social emotions, or social affective behavior, is a translationally important goal. The insular cortex is consistently implicated in stress-related social and anxiety disorders, which are associated with diminished ability to make and use inferences about the emotions of others to guide behavior. We investigated how corticotropin-releasing factor (CRF), a neuromodulator evoked upon exposure to stressed conspecifics, influenced the insula. We hypothesized that social affective behavior requires CRF signaling in the insular cortex in order to detect stress in social interactions. In acute slices from male and female rats, CRF depolarized insular pyramidal neurons. In males, but not females, CRF suppressed presynaptic GABAergic inhibition leading to greater excitatory synaptic efficacy in a CRF receptor 1 (CRF1)- and cannabinoid receptor 1 (CB1)-dependent fashion. In males only, insular CRF increased social investigation, and CRF1 and CB1 antagonists interfered with social interactions with stressed conspecifics. To investigate the molecular and cellular basis for the effect of CRF we examined insular CRF1 and CB1 mRNAs and found greater total insula CRF1 mRNA in females but greater CRF1 and CB1 mRNA colocalization in male insular cortex glutamatergic neurons that suggest complex, sex-specific organization of CRF and endocannabinoid systems. Together these results reveal a new mechanism by which stress and affect contribute to social affective behavior.

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“…Superadditive modulation of responses to pure tones by air puffs, following the principle of inverse effectiveness, has been observed in the insula of anesthetized mice ( Gogolla et al, 2014 ), indicating that classical MSI occurs in this region. Furthermore, neurons in the insula of male mice are modulated by social interaction with another male ( Miura et al, 2020 ). Nevertheless, the specific sensory inputs mediating this effect, as well as the involvement of the insula in mating behaviors, remain to be tested.…”

Section: Neural Circuitry For Integration Of Social Signalsmentioning

confidence: 99%

Cupid’s quiver: Integrating sensory cues in rodent mating systems

Hoglen

Manoli

2022

Front. Neural Circuits

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In many animal species, males and females exploit different mating strategies, display sex-typical behaviors, and use distinct systems to recognize ethologically relevant cues. Mate selection thus requires mutual recognition across diverse social interactions based on distinct sensory signals. These sex differences in courtship and mating behaviors correspond to differences in sensory systems and downstream neural substrates engaged to recognize and respond to courtship signals. In many rodents, males tend to rely heavily on volatile olfactory and pheromone cues, while females appear to be guided more by a combination of these chemosensory signals with acoustic cues in the form of ultrasonic vocalizations. The mechanisms by which chemical and acoustic cues are integrated to control behavior are understudied in mating but are known to be important in the control of maternal behaviors. Socially monogamous species constitute a behaviorally distinct group of rodents. In these species, anatomic differences between males and females outside the nervous system are less prominent than in species with non-monogamous mating systems, and both sexes engage in more symmetric social behaviors and form attachments. Nevertheless, despite the apparent similarities in behaviors displayed by monogamous males and females, the circuitry supporting social, mating, and attachment behaviors in these species is increasingly thought to differ between the sexes. Sex differences in sensory modalities most important for mate recognition in across species are of particular interest and present a wealth of questions yet to be answered. Here, we discuss how distinct sensory cues may be integrated to drive social and attachment behaviors in rodents, and the differing roles of specific sensory systems in eliciting displays of behavior by females or males.

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Encoding of social exploration by neural ensembles in the insular cortex

Cited by 27 publications

References 58 publications

The role of the anterior insula during targeted helping behavior in male rats

The role of the anterior insula during targeted helping behavior in male rats

Insular cortex corticotropin-releasing factor integrates stress signaling with social affective behavior

Cupid’s quiver: Integrating sensory cues in rodent mating systems

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