Neural signals implicated in the processing of appetitive and aversive events in social and non-social contexts

Vázquez, Daniela; Schneider, Kevin; Roesch, Matthew R.

doi:10.3389/fnsys.2022.926388

Cited by 3 publications

(2 citation statements)

References 211 publications

(318 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The addition of both supervised 34 and unsupervised [62][63][64] behavioral classification within the context of volitional social decision making has tremendous potential for resolving underlying neural mechanisms. Second, since OSS incorporates time-locked operant events, as well as discriminative and conditioned cues, physiological measurements and neural manipulations can be paired with discrete events within the OSS model to study neural circuitry during social reward behavior 65 .…”

Section: Discussionmentioning

confidence: 99%

Individual differences in volitional social motivation in male and female mice following social stress

Navarrete

Schneider

Smith

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

Background: A key challenge in developing new treatments for neuropsychiatric illness is the disconnect between preclinical models and the complexity of human social behavior. We aimed to integrate voluntary social self-administration into a preclinical rodent stress model, as a platform for the identification of basic brain and behavior mechanisms underlying stress-induced individual differences in social motivation. Here, we introduce an operant social stress (OSS) procedure with male and female mice, where lever presses are reinforced by freely moving social interaction with a familiar social partner across social stress exposure. Methods: OSS is composed of three phases: (i) social self-administration training, (ii) social stress concurrent with daily reinforced social self-administration testing, and (iii) post-stress operant social reward testing under both non-reinforced and reinforced conditions. We resolve social stress-induced changes to social motivation behaviors using hierarchical clustering and aggregated z-scores, capturing the spectrum of individual differences that we describe with a social index score. Results: OSS captures a range of stress-related dynamic social motivation behaviors inclusive of sex as a biological variable. Both male and female mice lever press for access to a social partner, independent of social partner coat color or familiarity. Social stress attenuates social self-administration in males and promotes social reward seeking behavior in females. Hierarchical clustering does not adequately describe the relative distributions of social motivation following stress, which we find is better described as a non-binary behavioral distribution that we define by introducing the social index score. This index is stable across individual mice. Conclusion: We demonstrate that OSS can be used to detect stable individual differences in stress-induced changes to social motivation in male and female mice. These differences may reflect unique neurobiological, cellular and circuit mechanisms not captured by preclinical models that omit voluntary social behaviors. The inclusion of volitional social procedures may enhance the understanding of behavioral adaptations promoting stress resiliency and their mechanisms under more naturalistic conditions.

show abstract

Section: Discussionmentioning

confidence: 99%

Individual differences in volitional social motivation in male and female mice following social stress

Navarrete

Schneider

Smith

et al. 2022

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…The anterior cingulate cortex (ACC) has been implicated across a plethora of cognitive functions—including attention and error detection ( Rescorla, 1973 ; D'Esposito et al, 1995 ; Carter et al, 1998 ; Botvinick et al, 1999 ; Carter et al, 1999 ; Barch, 2001 ; Braver, 2001 ; Paus, 2001 ; Botvinick et al, 2004 ; Holroyd et al, 2004 ; Kerns et al, 2004 ; Weissman, 2004 ; Yeung et al, 2004 ; Carter and Van Veen, 2007 ; Aarts et al, 2008 ; Totah et al, 2009 ; Koob and Volkow, 2010 ; Hayden et al, 2011 ; Lovstad et al, 2012 ; Hyman et al, 2013 ; Narayanan et al, 2013 ; Laubach et al, 2015 ; Newman et al, 2015 ; Vassena et al, 2017 ; Wu et al, 2017 ; Soltani and Izquierdo, 2019 ; Stolyarova et al, 2019 ; Brockett et al, 2020 ; Schneider et al, 2020 ; Vázquez et al, 2022 ; Ye et al, 2023 ). Consistent with this work, single-neuron studies have described correlates related to these functions ( Davis et al, 2000 ; Bryden et al, 2019 ; Seamans, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Optogenetic Inhibition of Rat Anterior Cingulate Cortex Impairs the Ability to Initiate and Stay on Task

Vázquez,

Maulhardt,

Stalnaker

et al. 2024

J. Neurosci.

Self Cite

View full text Add to dashboard Cite

Our prior research has identified neural correlates of cognitive control in the anterior cingulate cortex (ACC), leading us to hypothesize that the ACC is necessary for increasing attention as rats flexibly learn new contingencies during a complex reward-guided decision-making task. Here, we tested this hypothesis by using optogenetics to transiently inhibit the ACC while rats of either sex performed the same two-choice task. ACC inhibition had a profound impact on behavior that extended beyond deficits in attention during learning when expected outcomes were uncertain. We found that ACC inactivation slowed and reduced the number of trials rats initiated, and impaired both their accuracy and their ability to complete sessions. Further, drift-diffusion model analysis suggested that free-choice performance and evidence accumulation (i.e., reduced drift rates) were degraded during initial learning—leading to weaker associations that were more easily overridden in later trial blocks (i.e., stronger bias). Together, these results suggest that in addition to attention-related functions, the ACC contributes to the ability to initiate trials and generally stay on task.Significant StatementAttentional deficits and the ability to stay on task are defining hallmarks of some of the most prevalent and disruptive neuropsychiatric disorders. Here, we use an optogenetic approach and computational modeling to study how within-subject modulation of the anterior cingulate cortex (ACC) impacts the ability of rats to initiate and complete a complex reward-guided decision-making task. We found that on days in which the ACC was inhibited, the ability of rats to initiate and stay on task was impaired, as well as their task accuracy and ability to complete sessions.

show abstract

Nucleus accumbens core single cell ensembles bidirectionally respond to experienced versus observed aversive events

Dinckol,

Wenger,

Zachry

et al. 2023

Sci Rep

View full text Add to dashboard Cite

Fear learning is a critical feature of survival skills among mammals. In rodents, fear learning manifests itself through direct experience of the aversive event or social transmission of aversive stimuli such as observing and acting on conspecifics’ distress. The neuronal network underlying the social transmission of information largely overlaps with the brain regions that mediate behavioral responses to aversive and rewarding stimuli. In this study, we recorded single cell activity patterns of nucleus accumbens (NAc) core neurons using in vivo optical imaging of calcium transients via miniature scopes. This cutting-edge imaging methodology not only allows us to record activity patterns of individual neurons but also lets us longitudinally follow these individual neurons across time and different behavioral states. Using this approach, we identified NAc core single cell ensembles that respond to experienced and/or observed aversive stimuli. Our results showed that experienced and observed aversive stimuli evoke NAc core ensemble activity that is largely positive, with a smaller subset of negative responses. The size of the NAc single cell ensemble response was greater for experienced aversive stimuli compared to observed aversive events. Our results also revealed sex differences in the NAc core single cell ensembles responses to experience aversive stimuli, where females showed a greater accumbal response. Importantly, we found a subpopulation within the NAc core single cell ensembles that show a bidirectional response to experienced aversive stimuli versus observed aversive stimuli (i.e., negative response to experienced and positive response to observed). Our results suggest that the NAc plays a role in differentiating somatosensory experience from social observation of aversion at a single cell level. These results have important implications for psychopathologies where social information processing is maladaptive, such as autism spectrum disorders.

show abstract

Neural signals implicated in the processing of appetitive and aversive events in social and non-social contexts

Cited by 3 publications

References 211 publications

Individual differences in volitional social motivation in male and female mice following social stress

Individual differences in volitional social motivation in male and female mice following social stress

Optogenetic Inhibition of Rat Anterior Cingulate Cortex Impairs the Ability to Initiate and Stay on Task

Nucleus accumbens core single cell ensembles bidirectionally respond to experienced versus observed aversive events

Contact Info

Product

Resources

About