Faculty Opinions recommendation of Dynamic patterns of correlated activity in the prefrontal cortex encode information about social behavior.

Social interactions are crucial to the survival and well-being of all mammals, including humans. Although the prelimbic cortex (PL, part of medial prefrontal cortex) has been implicated in social behavior, it is not clear which neurons are relevant, nor how they contribute. We found that the PL contains anatomically and molecularly distinct subpopulations of neurons that target 3 downstream regions that have been implicated in social behavior: the nucleus accumbens (NAc), the amygdala, and the ventral tegmental area. Activation of NAc-projecting PL neurons (PL-NAc), but not the other subpopulations, decreased preference for a social target, suggesting an unique contribution of this population to social behavior. To determine what information PL-NAc neurons convey, we recorded selectively from them, and found that individual neurons were active during social investigation, but only in specific spatial locations. Spatially-specific inhibition of these neurons prevented the formation of a social-spatial association at the inhibited location. In contrast, spatially nonspecific inhibition did not affect social behavior. Thus, the unexpected combination of social and spatial information within the PL-NAc population appears to support socially motivated behavior by enabling the formation of social-spatial associations.

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Impaired Perception of Unintentional Transgression of Social Norms after Prefrontal Cortex Damage: Relationship to Decision Making, Emotion Recognition, and Executive Functions

Archives of Clinical Neuropsychology ◽

10.1093/arclin/acab078 ◽

2021 ◽

Author(s):

Riadh Ouerchefani ◽

Naoufel Ouerchefani ◽

Mohamed Riadh Ben Rejeb ◽

Didier Le Gall

Keyword(s):

Decision Making ◽

Prefrontal Cortex ◽

Social Behavior ◽

Theory Of Mind ◽

Social Norms ◽

Executive Functions ◽

Emotion Recognition ◽

Iowa Gambling Task ◽

Gambling Task ◽

Basic Emotions

Abstract Objective Patients with prefrontal cortex damage often transgress social rules and show lower accuracy in identifying and explaining inappropriate social behavior. The objective of this study was to examine the relationship between the ability to perceive other unintentional transgressions of social norms and both decision making and emotion recognition as these abilities are critical for appropriate social behavior. Method We examined a group of patients with focal prefrontal cortex damage (N = 28) and a group of matched control participants (N = 28) for their abilities to detect unintentional transgression of social norms using the “Faux-Pas” task of theory of mind, to make advantageous decisions on the Iowa gambling task, and to recognize basic emotions on the Ekman facial affect test. Results The group of patients with frontal lobe damage was impaired in all of these tasks compared with control participants. Moreover, all the “Faux-Pas”, Iowa gambling, and emotion recognition tasks were significantly associated and predicted by executive measures of inhibition, flexibility, or planning. However, only measures from the Iowa gambling task were associated and predicted performance on the “Faux-Pas” task. These tasks were not associated with performance in recognition of basic emotions. These findings suggest that theory of mind, executive functions, and decision-making abilities act in an interdependent way for appropriate social behavior. However, theory of mind and emotion recognition seem to have distinct but additive effects upon social behavior. Results from VLSM analysis also corroborate these data by showing a partially overlapped prefrontal circuitry underlying these cognitive domains.

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Perinatal THC exposure via lactation induces lasting alterations to social behavior and prefrontal cortex function in rats at adulthood

Neuropsychopharmacology ◽

10.1038/s41386-020-0716-x ◽

2020 ◽

Vol 45 (11) ◽

pp. 1826-1833

Author(s):

Andrew F. Scheyer ◽

Milene Borsoi ◽

Anne-Laure Pelissier- Alicot ◽

Olivier J. J. Manzoni

Keyword(s):

Prefrontal Cortex ◽

Social Behavior

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Microbiota-driven transcriptional changes in prefrontal cortex override genetic differences in social behavior

eLife ◽

10.7554/elife.13442 ◽

2016 ◽

Vol 5 ◽

Cited By ~ 118

Author(s):

Mar Gacias ◽

Sevasti Gaspari ◽

Patricia-Mae G Santos ◽

Sabrina Tamburini ◽

Monica Andrade ◽

...

Keyword(s):

Gene Expression ◽

Prefrontal Cortex ◽

Social Behavior ◽

Gut Microbiota ◽

Nod Mice ◽

Mouse Strains ◽

Social Avoidance ◽

Nonobese Diabetic ◽

Gene Environment ◽

Transcriptional Changes

Gene-environment interactions impact the development of neuropsychiatric disorders, but the relative contributions are unclear. Here, we identify gut microbiota as sufficient to induce depressive-like behaviors in genetically distinct mouse strains. Daily gavage of vehicle (dH2O) in nonobese diabetic (NOD) mice induced a social avoidance behavior that was not observed in C57BL/6 mice. This was not observed in NOD animals with depleted microbiota via oral administration of antibiotics. Transfer of intestinal microbiota, including members of the Clostridiales, Lachnospiraceae and Ruminococcaceae, from vehicle-gavaged NOD donors to microbiota-depleted C57BL/6 recipients was sufficient to induce social avoidance and change gene expression and myelination in the prefrontal cortex. Metabolomic analysis identified increased cresol levels in these mice, and exposure of cultured oligodendrocytes to this metabolite prevented myelin gene expression and differentiation. Our results thus demonstrate that the gut microbiota modifies the synthesis of key metabolites affecting gene expression in the prefrontal cortex, thereby modulating social behavior.

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Maternal Separation Modifies the Activity of Social Processing Brain Nuclei Upon Social Novelty Exposure

Frontiers in Behavioral Neuroscience ◽

10.3389/fnbeh.2021.651263 ◽

2021 ◽

Vol 15 ◽

Author(s):

Sara Mejía-Chávez ◽

Arturo Venebra-Muñoz ◽

Fabio García-García ◽

Aleph Alejandro Corona-Morales ◽

Arturo Enrique Orozco-Vargas

Keyword(s):

Prefrontal Cortex ◽

Nucleus Accumbens ◽

Social Behavior ◽

Medial Prefrontal Cortex ◽

Paraventricular Nucleus ◽

Maternal Separation ◽

Lateral Septum ◽

Medial Amygdala ◽

Physiological Basis ◽

Brain Nuclei

Maternal separation has been shown to disrupt proper brain development and maturation, having profound consequences on the neuroendocrine systems in charge of the stress response, and has been shown to induce behavioral and cognitive abnormalities. At the behavioral level, maternal separation has been shown to increase offensive play-fighting in juvenile individuals and reduce social interest in adulthood. Since most of the studies that have evaluated the consequences of maternal separation on social behavior have focused on behavioral analysis, there is a need for a further understanding of the neuronal mechanisms underlying the changes in social behavior induced by maternal separation. Therefore, the aim of the present research was to assess the long-term effects of maternal separation on social interaction behavior and to assess the activity of several brain regions involved in the processing of social cues and reward upon social novelty exposure, using c-Fos immunohistochemistry as a marker of neuronal activity. Male Wistar rats were subjected to 4 h maternal separation during the neonatal period, 9:00 h–13:00 h from postnatal day 1 to 21, and exposed to social novelty during adulthood. After social novelty exposure, brains were fixed and coronal sections of the medial amygdala, lateral septum (LS), paraventricular nucleus of the hypothalamus, nucleus accumbens, and medial prefrontal cortex were obtained for c-Fos immunohistochemistry. Maternally separated rats spent less time investigating the novel peer, suggesting that maternal separation reduces social approach motivation. Furthermore, maternal separation reduced the number of c-Fos positive cells of the medial amygdala, paraventricular nucleus of the hypothalamus, LS, nucleus accumbens, and medial prefrontal cortex upon social novelty exposure. These findings suggest that maternal separation can reduce the plastic capacity of several brain nuclei, which constitute a physiological basis for the emergence of behavioral disorders presented later in life reported to be linked to early life adversity.

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Dynamic patterns of correlated activity in the prefrontal cortex encode information about social behavior

10.1101/2020.08.05.238741 ◽

2020 ◽

Author(s):

Nicholas A. Frost ◽

Anna Haggart ◽

Vikaas S. Sohal

Keyword(s):

Neural Network ◽

Social Behavior ◽

New Technologies ◽

Activity Levels ◽

Specific Mechanism ◽

Individual Activity ◽

Neuronal Ensembles ◽

Disease States ◽

Correlated Activity ◽

Neural Network Classifiers

ABSTRACTNew technologies have made it possible to measure activity from many neurons simultaneously. Nevertheless, most studies still analyze the activity of simultaneously recorded neurons one-at-a-time, then group together neurons which increase their activity during similar behaviors into an ‘ensemble.’ This notion of an ensemble ignores the ability of neurons to act collectively, and encode and transmit information in ways that are not reflected by their individual activity levels. We used microendoscopic GCaMP imaging to measure prefrontal activity while mice were either alone or engaged in social interaction. We developed new approaches, using neural network classifiers and surrogate (shuffled) datasets, to characterize how neurons synergistically transmit information about social behavior. Surrogate datasets which preserve behaviorally-specific patterns of coactivity (correlations) outperform those which preserve behaviorally-driven changes in activity levels but not correlated activity. This shows that prefrontal neurons act collectively to transmit information about socialization, because social behavior elicits increases in correlated activity that are not explained simply by the activity levels of the underlying neurons. Notably, this ability of correlated activity to enhance the information transmitted by neuronal ensembles is lost in mice lacking the autism-associated gene Shank3. These results show that synergy is an important concept for the coding of social behavior which can be disrupted in disease states, reveal a specific mechanism underlying this synergy (social behavior increases correlated activity within specific ensembles), and outlines methods for studying how neurons within an ensemble can work together to encode information.

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Prefrontal cortical control of a brainstem social behavior circuit

10.1101/073734 ◽

2016 ◽

Cited By ~ 1

Author(s):

Tamara B. Franklin ◽

Bianca A. Silva ◽

Zina Perova ◽

Livia Marrone ◽

Maria E. Masferrer ◽

...

Keyword(s):

Prefrontal Cortex ◽

Social Behavior ◽

Neural Circuits ◽

Critical Role ◽

Social Defeat ◽

Selective Inhibition ◽

Behavioral Adaptation ◽

Cortical Control ◽

Prefrontal Cortical ◽

Defensive Responses

SummaryThe prefrontal cortex plays a critical role in adjusting an organism’s behavior to its environment. In particular, numerous studies have implicated the prefrontal cortex in the control of social behavior, but the neural circuits that mediate these effects remain unknown. Here we investigated behavioral adaptation to social defeat in mice and uncovered a critical contribution of neural projections from the medial prefrontal cortex to the dorsal periaqueductal grey, a brainstem area vital for defensive responses. Social defeat caused a weakening of functional connectivity between these two areas and selective inhibition of these projections mimicked the behavioral effects of social defeat. These findings define a specific neural projection by which the prefrontal cortex can control and adapt social behavior.

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