Posters

Effects of adolescent social trauma on social behaviour and the oxytocin system in mice 

Melanie Kabas, Leopold Kinzel, Anna Bludau, Inga D. Neumann. 

Adolescence is a critical developmental phase of high susceptibility to mental disorders, including social anxiety disorder (SAD). Oxytocin (OXT), a neuropeptide known for its pro-social and anxiolytic attributes, is a therapeutic option for SAD patients and has been described to reverse social fear in adult male and female mice specifically within the lateral septum (Zoicas et al. 2014; Menon et al. 2018). In this context, OXT signalling in the ventromedial hypothalamus (VMH) may also be relevant, as shown in social defeat-induced social avoidance learning (Osakada et al. 2022). However, the role of OXT receptors (OXTR) in the VMH in the modulation of social fear remains to be elucidated.Here, we studied the acute and long-lasting consequences of social trauma in adolescent male and female mice on social behaviour and the OXT system using the social fear conditioning (SFC) paradigm (Toth et al. 2012; Menon et al. 2018). This model of SAD is based on operant conditioning principles, as mice receive a mild (0.7mA) electric foot shock upon interaction with a social stimulus (SFC+), whereas controls can interact freely without punishment (SFC-). To analyse OXTR binding by means of receptor autoradiography, mice conditioned during adolescence were exposed to a singular social stimulus 1d or 28d post-acquisition. Here, male and female mice expressed social avoidance when exposed to a social stimulus 1d post-acquisition, whereas only male mice showed social avoidance when exposed 28d later. We further revealed reduced OXTR binding in the VMH when exposing male SFC+ mice to a social stimulus 28d post-acquisition compared to respective SFC- controls. Utilizing immunohistochemical stainings (IHC) and RNAscope, we identified OXTergic projections in close proximity to OXTR-positive neurons in the ventrolateral VMH. These OXT inputs originate from the paraventricular nucleus of the hypothalamus (PVN) as identified by retrograde tracing. Thus, our findings suggest that adolescent social trauma induces alterations of the OXT system, particularly within the PVN, which might contribute to persistence of social fear in male mice. However, using IHC for cFos, we found no alterations in the activation of PVN OXT cells in response to adolescent SFC in male and female mice. To investigate the functional impact of OXT within the VMH on social fear in general we bilaterally infused OXT (5ng/ 0.2μl/ side) into the VMH of adult SFC+ male mice 10 min prior to social fear extinction. However, we could not reveal any effects on social investigation.In conclusion, exposure to adolescent social trauma induces robust social fear in male and female mice, which lasts until adulthood only in male mice and is accompanied by alterations in OXTR binding within the VMH. However, conclusive evidence for the involvement of the OXTergic PVN-VMH circuit in the regulation of social fear is still missing.

Intergenerational transmission of social fear in male mice

Laura Stangl, Anna Bludau, Inga Neumann, and Rohit Menon

Several rodent studies have shown that stressful and traumatic experiences of the F0 generation can be transmitted to often lead to behavioral perturbations in the forthcoming generation. For instance, social trauma introduced by chronic social defeat stress changes depression- and anxiety-like behavior in the following generation compared to non-stressed controls (Dietz et al., 2011). Similarly, acute olfactory fear conditioning is also known to induce enhanced startle responses in the subsequent F1 and F2 generations (Dias and Ressler, 2014). However, the transmission of behavioral alterations induced by acute social trauma across generations has not yet been studied. To this end, we used the social fear conditioning (SFC) paradigm that generates robust social avoidance in male and female mice as a source of social trauma and examined its behavioral effects across 3 generations in mice. SFC is an operant conditioning-based paradigm that pairs foot shocks with social contact as a proxy for an aversive or traumatic social experience in mice (Toth et al., 2012). The social fear conditioning paradigm has two basic groups: The conditioned group (SFC+), which receives a foot shock when approaching the social stimulus, and the unconditioned/control group (SFC-), which undergoes the same procedure but can freely explore the social stimulus without punishment.To study the transmission of social trauma-related behavioral changes, social fear acquisition was performed on male CD1 mice (F0) that were subsequently mated with naïve female CD1 mice. After impregnation, the F0-SFC+ and SFC- males were separated and tested for their naturally occurring social preference using a 3-chambered preference apparatus. F0-SFC+ males showed social avoidance during the preference test, confirming conditioning success. Their F1 offspring was tested at the age of eight weeks for various behavioral and molecular parameters. Both male and female F1-SFC+ offspring showed no alteration in anxiety-like behavior tested in the elevated plus maze (EPM), light dark box (LDB), open field test (OFT), and novel object recognition (NOR) compared to the respective SFC- group. However, the male offspring of SFC+ fathers showed a lack of innate social preference, whereas the female offspring exhibited social preference similar to the SFC-control group. As a possible brain region involved in the expression of the behavioral changes, we focused on the lateral septum (LS) because of its known involvement in regulating social behavior (Menon et al., 2022). Utilizing a PCR-Array for synaptic plasticity, we could find several possible target genes, such as Mapk1, Plcg1 or Adcy8, that might be involved in transmitting these behavioral changes.In conclusion, we could show that the social avoidance introduced in F0 leads to altered social behavior in male F1 offspring. Furthermore, we found promising target genes that might be involved in the transmission of this phenotype. However, further research must be conducted to shed light on specific epigenetic mechanisms underlying the transmission of reduced social preference across generations.

The role of the dorsomedial column of the periaqueductal gray in the social defensive behavior of Wistar male rats

Alisson Pinto de Almeida; Alicia Moraes Tamais; Carolina Zerbini; Fernando Falkenburger Melleu; Newton Sabino Canteras; Simone Cristina Motta

The periaqueductal grey matter (PAG) is an essential midbrain structure for defensive responses against a range of threats, innate or not. Previous work from our laboratory suggests that the dorsomedial column of the rostral PAG (rPAGdm) participates in the organization of the defensive response against aggressive conspecifics. The rPAGdm receives inputs from the dorsal premammillary nucleus of the hypothalamus (PMD), important for developing passive defense behavior. In the present work, we aimed to investigate the role of rPAGdm in social defense by evaluating the effects of bilateral lesions of the rPAGdm on the defensive behavior of Wistar male rats. For this, a solution of NMDA (n=6) or saline (n=6) was deposited bilaterally in the rPAGdm of Wistar rats. Two weeks after surgery, these animals were submitted to the resident-intruder paradigm. In general, lesioned rats spent more time on exploratory behavior than intact animals (intact: 25.33±26.22 s; NMDA rPAGdm lesion: 104.33±39.57 s; t(df=10)=-4.08, p=0.002). Also, we observed a reduction in the time spent on passive defense in lesioned rats (intact: 185.33±69.93 s; NMDA rPAGdm lesion: 10.50±8.83 s; t(df=10)=6.08, p<0.001). Concerning social behavior, active defense, and other behaviors, we did not observe differences between groups (p>0.01). Our data suggests that rPAGdm is an important region for the expression of passive defense during an encounter with an aggressive conspecific, and could be an important output of information from the PMD.

Connections of the dorsomedial division of rostral periaqueductal grey matter: implications for social defeat in rats

Alicia Moraes Tamais, Alisson Pinto de Almeida, Carolina Zerbini, Fernando Falkenburger Melleu, Newton Sabino Canteras, Simone Cristina Motta

Social defense is an essential behavior for the survival of an individual and consists of defensive behaviors carried out during the dispute between conspecifics for territory, resources, and reproductive partners. The periaqueductal gray (PAG) is a region downstream of the hypothalamic conspecific responsive circuit, which is involved in a variety of behaviors, including social defense. In this work, we investigated the role of the rostral part of the dorsomedial PAG (rPAGdm) in social defense by evaluating the activity pattern of different sources of inputs to this region during social defeat. For this, we made iontophoretic deposits of Fluoro Gold (FG) unilaterally into the rPAGdm of Wistar male rats (n=4). One week later, these animals were subjected to the resident-intruder paradigm. Then, the brains were processed to evaluate the expression of Fos and FG. We also evaluated the outputs of rPAGdm by injecting the anterograde tracer Phaseolus vulgaris–leucoagglutinin (PHA-L) into the rPAGdm of Wistar male rats (n=4). Briefly, our tracing study suggests that rPAGdm is not only a relay of hypothalamic information to downstream regions but also a node in a feedback-loop circuit for social defense. This circuit consists of a loop between the anterior part of the anterior hypothalamic nucleus (AHNa), dorsal premammilary nucleus (PMD), rPAGdm, and cuneiform nucleus (CUN). The rPAGdm can also receive different types of information related to the aversive context as visual (by the ventromedial part of the lateral geniculate nucleus - LGvm), nociceptive (by the caudal part of the lateral parabrachial nucleus - PBlc), and contextual (by the juxtaparaventricular part of the lateral hypothalamic area - LHAjp). Also, the dorsal part of the anterior cingulate area (ACAd) inputs can be important for the acquisition of social fear memory. Thus, our results support that rPAGdm mediates social defensive responses through ascending paths to prosencephalic circuits likely mediated by the CUN.

Wildtype peers rescue social play communication deficits in juvenile female Cacna1c heterozygous rats

Theresa M. Kisko, Rebecca Bogdan, Rukhshona Kayumova, Rainer K.W. Schwarting, Markus Wöhr

Early social practices and experiences are crucial for promoting healthy brain development. The CACNA1C risk gene has been linked to various neuropsychiatric disorders characterized by social functioning and communication deficits. In this study, we examined the impact of social environment and play partner genotype on social play and 50-kHz USV emission in juvenile female rats. We housed them in cages with either same-genotype or mixed-genotype partners and observed their behavior during social play with a partner of the same or opposite genotype. The results indicate that social environment and play partner genotype can influence social play and 50-kHz USV emission. The heterozygous Cacna1c (HET) females require experience with a wildtype Cacna1c (WT) play partner to exhibit comparable levels of play and 50-kHz USV emission. Same-genotype HET pairs played less and emitted fewer 50-kHz USV than same-genotype WT or opposite-genotype pairs. However, we discovered that playing with a WT partner can rescue the decrease in social play and 50-kHz USV emission in HET pairs. Notably, when the first play partner was WT, subsequent interactions with ensuing partners resulted in increased play and 50-kHz USV emission. These findings suggest that the genetic makeup of the social environment and/or social peers can influence social play in Cacna1c+/− haploinsufficient rats. Specifically, our results indicate that WT peers can help improve behavior and communication in Cacna1c female rats. These findings have significant implications as they demonstrate that the genetic makeup of the social environment can affect the phenotypic changes in genetic rat models of neuropsychiatric disorders.

Ultrasonic Vocalizations and Social Behavior in Mouse Models for Autism Spectrum Disorder

A. Özge Sungur, Martin Lackinger, Rainer K.W. Schwarting, Marco B. Rust, Gerhard Schratt, Markus Wöhr

Autism Spectrum Disorder (ASD) is a group of neurodevelopmental disorders characterized by persistent deficits in social communication and interaction across multiple contexts, and restricted, repetitive patterns of behavior. Several studies highlight immense contribution of genetic factors to disease etiology. Mouse models provide excellent translational tools to discover disease pathogenesis underlying behavioral and neurobiological abnormalities. Mice communicate using olfactory social signals and emitting ultrasonic vocalizations (USV) in various situations, depending on age, environment, and genetic factors. Measuring USV at different stages of development and experimental contexts is therefore a useful tool to bring about the communication deficits in mouse models. In fact, alterations in ultrasonic communication have been reported in several mouse models for neurodevelopmental disorders, offering reasonable face validity to diagnostic symptoms of ASD. The results I would like to present focus on a wide repertoire of mouse vocalizations, emphasizing the communicative function of these under various contexts. In order to give insights into their significance in neurodevelopmental disorders, I will provide examples of USV alterations in mouse models for neurodevelopmental disorders and their link to social behavior, specifically in mice lacking proteins that act as mediators of dendritic spine formation.

Bridging in vivo immunohistochemical study and in vitro electrophysiological study: ERK activation is induced by olfactory nerve inputs and acetylcholine in rat olfactory bulb vasopressin cells

Hajime Suyama1, Lisa Kindler2, Michael Lukas2, Esteban Pino2, Veronica Egger2

1Biology of neural circuits, Institute of Biology, Otto-von-Guericke University Magdeburg, Germany

2Neurophysilogy, Institute of Zoology, University of Regensburg, Germany

Vasopressin is a neuropeptide involved in various social behaviors and is functionally essential for social discrimination in rats in the olfactory bulb (OB), the brains first relay station for olfactory processing. We previously showed that vasopressin cells (VPCs) in acute OB slices respond to electrical olfactory nerve stimulation with hyperpolarization, and that acetylcholine (ACh) application switches this evoked inhibition to action potential firing in the majority of cells. Moreover, we found that more VPCs express the neural activity marker  pERK in behaving rats that are exposed to conspecifics in comparison to the control group. However, whether VPC action potential firing in OB slices in the presence of ACh and increased ERK it is unclear if activation during social interaction can be actually mapped onto each other. Therefore, we investigated pERK activation in acute OB slices from transgenic VP-eGFP rats with either chemical or olfactory nerve stimulation using immunohistochemistry against pERK and GFP. Neither KCl nor NMDA application increased percentages of pERK-positive VPCs. In line with our previous observation, olfactory nerve stimulation alone also had no effect whereas olfactory nerve stimulation in the ACh condition increased percentages of pERK-positive VPCs. Our results suggest that chemical general stimulation of the OB which directly stimulates VPCs as well, is not enough to activate pERK in VPCs. Moreover, as shown previously in electrophysiological experiments, this study indicates that external neuromodulation, e.g. through ACh, is necessary for olfactory nerve stimulation to activate VPCs. Taken together, we suggest that afferent-evoked VPC action potential firing is a prerequisite for the pERK activation caused by coincident sensory and ACh neuromodulatory input, even though spiking alone not always appears to be visible as pERK activation.

Auditory response in the posterior intralaminar thalamus for maternal behavior 

Mingyu Yang & Silvana Valtcheva

Infant-oriented maternal behavior is often driven by the multimodal sensory signals that offspring emit to communicate their physiological needs. Stereotypical patterns of maternal behavior in mice include staying in the nest to nurse and retrieving misplaced pups back to the nest. Nursing is predominantly triggered by somatosensory input during maternal-pup contact, whereas pup retrieval is elicited by specific auditory cues, such as distress vocalizations when pups are isolated outside the nest. However, the simultaneous presence of auditory and somatosensory pup cues may lead to a competition for maternal care. Therefore, understanding the neural substrate underlying multisensory processing of competing infant cues is critical to ensure the survival and well-being of all offspring. One potential neural hub for processing infant cues is the posterior intralaminar complex of the thalamus (PIL). PIL receives auditory inputs from the inferior colliculus and primary auditory cortex, as well as somatosensory inputs from the spinal cord. Notably, silencing PIL via chemogenetic methods prevents dams from responding to pup distress calls and searching for the isolated pup (Valtcheva et al., 2023). Furthermore, within PIL, a specific subpopulation of neurons expressing calbindin (CB, PILcb) is known to be particularly activated during maternal behaviors. Therefore, we aimed to elucidate the responsiveness of PILcb neurons to auditory pup cues, especially in the presence of competing somatosensory cues, and its influence on pup-oriented maternal behaviors. To achieve this goal, we performed whole-cell current-clamp recordings from tdTomato-positive PILcb neurons in acute brain slices from Calbindin-Cre x Ai14 female mice. We characterized and compared the intrinsic properties and excitability of PILcb neurons in virgin and maternal mice. In addition, we examined the spiking output of PILcb neurons in response to extracellular stimulation at different frequencies, which may help to identify their preferred firing frequencies and their suitability for processing and relaying pup-related auditory information. We observed that PILcb neurons exhibited slightly higher excitability in dams compared to virgins. Furthermore, we found that PILcb neurons displayed a preference for 5 Hz stimulation, which falls within the frequency range of pup calls.

What’s so funny? Long-term effects of tickling-induced “rat laughter” on cognitive performance.

Elisabeth Skorobogatov, Ellen Dotselaere, Markus Wöhr

Rats are known to emit a wide array of ultrasonic vocalizations. A substantial body of evidence supports their reflectance of various emotional states. While a debate exists regarding the classification of these vocalizations, a consensus generally recognizes three primary types: 40-kHz pup calls signaling need for maternal care, 22-kHz calls indexing negative affect, and 50-kHz calls associated with positive affect. One of most efficient ways of inducing 50-kHz vocalizations is mimicking rough-and-tumble play, a well-established source of reward in rats, through tickling by human experimenters. It was previously shown that tickling-induced 50-kHz calls result in increased hippocampal neurogenesis. Because hippocampal neurogenesis was repeatedly linked with memory, it was therefore speculated that tickling leads to higher cognitive performance. In this study, we investigated the impact of tickling-induced vocalizations on cognitive performance by comparing tickled to non-tickled Sprague-Dawley rats. Cognition was assessed through two hippocampal-dependent paradigms: a spatial learning experiment using the eight-armed radial maze and a passive avoidance test. Our findings demonstrate that tickling enhanced the emission appetitive 50-kHz vocalizations. In addition, tickling-induced 50-kHz calls were found to have distinct acoustic characteristics; including longer call duration, higher amplitude, and reduced frequency modulation compared to the 50-kHz calls from non-tickled rats. While tickling did not exhibit significant effects on spatial learning abilities, it did foster enhanced cognitive flexibility during the acquisition of the maze configuration, as well as stronger acquired passive avoidance responses. This study offers valuable insights into the intricate relationship between affect-related vocalizations and cognitive performance in rats. 

A galanin-positive population of lumbar spinal cord neurons modulates sexual excitation and copulatory behavior

Ana Rita P. Mendes, Constanze Lenschow, Liliana Ferreira, Bertrand Lacoste, Camille Quilgars, Sandrine S. Bertrand and Susana Q. Lima

In mammals, copulatory behavior involves a series of actions that bring the male to the ejaculatory threshold, allowing genital stimulation to trigger ejaculation. While copulation and sexual excitation are thought to be centrally regulated, ejaculation is a reflex controlled by a spinal circuit whose activity is strongly inhibited by descending input from the brain, bearing no role on the regulation of copulatory behavior until the ejaculatory threshold is reached. However, this hypothesis remains untested. To address this question, we combined genetic approaches with electrophysiological and behavioral analysis to functionally map the mouse spinal circuit controlling the main muscle involved in sperm expulsion, the bulbospongiosus muscle (BSM). We found that BSM motor neurons (BSM-MNs) receive direct synaptic input from a group of galanin-expressing (Gal+) interneurons located in the upper lumbar spinal cord. Furthermore, the Gal+ population is progressively activated during sexual behavior and is activated by stimulation of the genital region. Electrical and optogenetic activation of the Gal+ neurons evoked activity in BSM-MNs and BSM after spinalization. Interestingly, these effects were dependent on the behavioral state of the male prior to spinalization and drastically decreased with repeated stimulation. Moreover, genetic ablation of the Gal+ neurons severely impacted the latency to ejaculate and the copulatory sequence. Taken together, our results imply an unexpected involvement of the spinal cord in the control of copulatory behavior and sexual excitation.

A Neuroanatomical Substrate for the Control of Female Sexual Rejection

Inês C. Dias1, Basma F. A. Husain2, Liliana Ferreira1, Ana Rasteiro1, Nicolas Gutierrez-Castellanos1, Susana Q. Lima1

1-Champalimaud Research, Champalimaud Centre for the Unknown, Avenida Brasília, Doca de Pedrouços, 1400-038, Lisboa, Portugal

2-The Francis Crick Institute, 1 Midland Road, London, NW1 1AT, United Kindgom

Selecting an appropriate behavioral response in an internal state dependent manner is fundamental for well-being. Throughout the reproductive cycle, fluctuating levels of sex hormones coordinate female behavior with their reproductive capacity by modulating the activity of neuronal circuits expressing their specific receptors. Within the ventrolateral part of the ventromedial hypothalamus (VMHvl), neurons expressing receptors for sex hormones play a crucial role in female sexual receptivity. However, recent findings show that cellular, transcriptomic and functional properties of the VMHvl neurons are heterogeneous, varying along the anterior-posterior axis. While the progesterone-expressing neurons of the VMHvl (VMHvl.PR+) have been shown to be active when the female is receptive and mating, in our laboratory, using in vivo calcium imaging and optogenetics we show that the anterior VMHvl.PR+ neurons are involved in rejection behavior when the female is non-receptive.

Using viral tracing techniques we found that although both subpopulations strongly project to the periaqueductal gray (PAG), their connectivity patterns into this midbrain structure differ across its AP axis, with aVMHvl.PR+ neurons preferentially projecting to medial and posterior subregions, while the terminals of pVMHvl.PR+ neurons are detected posteriorly. Furthermore, the artificial activation of aVMHvl.PR+ neurons lead to activation of specific PAG subregions. Given the established role of the PAG in the control of opposing behaviors, such as escape and immobility, we hypothesize that the changes in female sexual behavior are in part controlled by the combinatorial action of the two PR+ populations on the PAG. We are currently testing this hypothesis by manipulating the activity of PR+ terminals in the PAG, hoping to further our understanding of such important behavior.

Social memory alterations, increased anxiety and impaired working memory in a forebrain GABAergic interneuron-specific mouse model of RASopathies

Jeimmy Ceron, Gürsel Çalışkan, Oliver Stork

RASopathies are a family of developmental disorders that affect approximately 1 in 1000 individuals and are caused by germline mutations in genes encoding components of the Ras-MAPK pathway. Patients have a higher probability of experiencing neuropsychological impairments such as cognitive disabilities, language deficits, and social and emotional challenges. Although alterations in cognitive abilities have been considerably characterized in different mouse models of RASopathies, dysregulations in social and emotional behaviors and their underlying neuronal mechanisms have not been rigorously explored yet. Therefore, a conditional mouse line was established with a selected knock-in hyperactivating mutation of the BRAF gene (central component of the Ras-MAPK pathway) exclusively in forebrain GABAergic interneurons (BRAFQ241Rfloxed/wt-DLX5-6Cre/+ or DBRAF mice) and its effects on social, emotional, and cognitive behaviors were characterized. These DBRAF mice exhibit a specific impairment in social recognition memory in the three-chamber sociability test without a general change in sociability. Additionally, they exhibit a pronounced anxiety phenotype in the elevated plus maze and open field tasks, as well as a deficit in working memory in the Y-maze. A c-Fos mapping revealed a reduced behaviorally induced activation in the dentate gyrus and CA3 subregions of the dorsal hippocampus. The density of GABAergic synapses and of specific interneuron populations however proved to be largely unchanged. These results reveal a potential role of the Ras-MAPK signaling in GABAergic interneurons in the emergence of social, emotional, and cognitive dysfunctions. Supported by the Federal Ministry of Education and Research, Germany, Project GeNeRARe.

DREADD-mediated amygdala activation is sufficient to induce anxiety-like responses in young nonhuman primates

Sascha A. L. Mueller, Jonathan A. Oler, Nakul Aggarwal, Patrick H. Roseboom, Marissa K. Riedel, Victoria R. Elam, Miles E. Olsen, Alexandra H. DiFilippo, Bradley T. Christian, Xing Hu, Adriana Galvan, Matthew A. Boehm, Mike Michaelides, Ned H. Kalin

Anxiety disorders are among the most prevalent psychiatric disorders, with symptoms often beginning early in life. To model the pathophysiology of human pathological anxiety, we utilized Designer Receptors Exclusively Activated by Designer Drugs (DREADDs) in a nonhuman primate model of anxious temperament to selectively increase neuronal activity of the amygdala. Subjects included 10 young rhesus macaques; 5 received bilateral infusions of AAV5-hSyn-HA-hM3Dq into the dorsal amygdala, and 5 served as controls. Subjects underwent behavioral testing in the human intruder paradigm following clozapine or vehicle administration, prior to and following surgery. Behavioral results indicated that clozapine treatment post-surgery increased freezing across different threat-related contexts in hM3Dq subjects. This effect was again observed approximately 1.9 years following surgery, indicating the long-term functional capacity of DREADD-induced neuronal activation. [11C]deschloroclozapine PET imaging demonstrated amygdala hM3Dq-HA specific binding, and immunohistochemistry revealed that hM3Dq-HA expression was most prominent in basolateral nuclei. Electron microscopy confirmed expression was predominantly on neuronal membranes. Together, these data demonstrate that activation of primate amygdala neurons is sufficient to induce increased anxiety-related behaviors, which could serve as a model to investigate pathological anxiety in humans.

Distinct decision processes for 3D and motion visual stimuli in humans and macaques

Revan Rangotis, Sabina Nowakowska, Peter Dayan, Ehsan Kakaei, Abibat Akande and Kristine Krug

Neurophysiology localised perceptual decision signals for binocular 3D depth and motion stimuli to visual area V5/MT. Drift diffusion modelling (DDM) is widely used to investigate the underlying decision-making processes by simulating decisions as noisy evidence-accumulation which terminates once a threshold is crossed. Two key questions remain unexplored: 1. To what extent are modelled decision processes affected by the visual stimulus (here 3D depth vs. motion) and by the effector for the response (hand vs. saccades)? 2. Are the modelling parameters comparable between monkeys and humans? To answer these questions, we tested 2 male monkeys (Macaca mulatta) and 20 humans (13 females, 7 males, aged 18-40, mean age 29.6, range 18-40 years) on different stimulus/effector combinations in a 2-alternative forced-choice task. Stimuli were a 3D structure-from-motion cylinder or a random dot kinematogram (RDK), requiring perceptual decisions about binocular depth or direction of motion, respectively. Effectors comprised hand and saccadic eye movements. Monkeys only performed the cylinder task with saccadic responses and the RDK task with hand movements, whereas humans performed all combinations in a counterbalanced order. Psychophysical performance and reaction times were comparable between species on the same task. The parameter distributions of a hierarchical DDM model (distance to bound, non-decision time, drift-rate slope, drift-rate intercept, bias) indicated a difference in distance to bound specific to the visual stimulus in both species. Using dimensionality reduction, linear discriminant analysis (LDA) revealed a strong separation by stimulus type but not for the effector for the human data (p<0.001, ROC analysis). Similar clustering was observed for the monkey data when it was projected onto the same space. We conclude that the DDM reveals distinct brain processes for perceptual decisions about visual motion and binocular 3D stimuli in humans and macaques, although perceptual signals for both have been localised to the same brain area. We found no distinction between hand and eye movement responses in either species.

Segregated divisions of macaque lateral intraparietal area (LIP) revealed by post-mortem diffusion-weighted imaging and tractography

Wirsum M.J.1,6 Smith J.E.T.2,3, Dyrby T.B.4,5, Krug K.1,2,6

1Institute of Biology, Otto-von-Guericke-University Magdeburg, Germany. 2 DPAG, University of Oxford. 3Ernst Strüngmann Institute for Neuroscience with Max Planck Society, Frankfurt, Germany. 4Danish Research Centre for Magnetic Resonance, Copenhagen University Hospital, Denmark. 5Department of Applied Mathematics and Computer Science, Technical University of Denmark. 6 CIRC, Deutsches Zentrum für psychische Gesundheit, Magdeburg, Germany.

Lateral intraparietal area (LIP) plays a central role in the sensorimotor-transformations for targeting eye movements and spatial attention. Anatomically, LIP consists of two distinct regions: a heavily myelinated ventral region (LIPv) and a sparsely myelinated dorsal region (LIPd). LIPv and LIPd are associated with different functions and differ in their connectivity patterns with other brain areas. For now, these subdivisions can only be clearly delineated with histological approaches.

We investigated whether LIP can be divided into LIPd and LIPv based on their differential connectivity profiles with other areas, using high resolution diffusion weighted imaging (DWI) data and probabilistic tractography obtained from 4 post mortem rhesus macaque brains (2 females, 2 males, mean age = 8.75 ± 3.20 years). After systematic analysis of histological data from 25 publications, evaluating 39 potential target areas, six areas were chosen for tractography because of their robust connectivity with predominantly one of the two LIP regions: dorsal visual stream areas V3A, V6A and V5/MT, primarily connected to LIPv, and ventral visual stream areas IPa, TEm and V4d, mainly connected to LIPd. Tractography was run using FSL on the pre-processed, diffusion-modelled data to estimate the white matter tracts from LIP to the targets. Based on the relative strength of connectivity to these targets, LIP was then hardsegmented.

Qualitatively, LIP was divided in 6 out of 8 hemispheres into a more dorsal and more ventral part, which overlapped to a large extent with the ground-truth histological D99 atlas. When individual maps were randomly permuted 10,000 times, 7 out of 8 predicted maps performed better than chance (p < 0.025). The mean match with ground-truth for LIPv was 74.7% (STD = 8.9 %) and for LIPd 62.0% (STD = 21.2 %).

Excluding targets in individual hemispheres based on anatomical plausibility did not lead to significantly improved results (LIPv: p = 0.813; LIPd: p = 0.63, Wilcoxon signed-rank test).

We show that non-invasive DWI with probabilistic tractography can reliably segment parietal area LIP and potentially other cortical areas into their structural subdivisions in individual subjects based solely on connectivity. As next step, this approach is being applied to in vivo macaque and human brains to define subregions and circuits in individual subjects for research and clinical applications.

Keywords: connectivity, neuroanatomy, parietal cortex, MRI, sensorimotor cortex

Histological validation of diffusion MRI and tractography for tracing fibre tracts in macaque extrastriate visual cortex.

 *D. L. N. SAMS 1, J. E. T. SMITH 2,3 , C. GAILLARD 1, A. BASHIR 3, H. BRIDGE 4, T. B. DYRBY 5, K. KRUG 1;

1 Otto von Guericke Univ., Magdeburg, Germany; 2 Ernst Strüngmann Inst. (ESI) for Neurosci., Frankfurt, Germany; 3 Dept. of Physiology, Anat. and Genetics, Univ. of Oxford, Oxford OX1 3PT, UK., Oxford, United Kingdom; 4 Clin. Neurol., Univ. of Oxford, Oxford, United Kingdom; 5 Danish Res. Ctr. for Magnetic Resonance, Ctr. for Functional and Diagnos. Imaging and Research, Copenhagen Univ. Hospital, Amager & Hvidovre, Hvidovre, Copenhagen, Denmark

Diffusion-weighted magnetic resonance imaging (dMRI) with probabilistic tractography can non-invasively map white matter connectivity in human and animal brains, but it remains unclear how well this method captures underlying fibre tracts. We quantitatively compare specific white matter tracts labelled from a small cortical tracer injection site with tractography streamlines generated from the same cortical site.Biotinylated dextran amine (BDA) tracer (200 nL) was placed into the left extrastriate visual area V5/MT of two anaesthetized macaque monkeys, one male (M127), one female (M131). Ten to fifteen days after the injection, monkeys (mean age 9.3 years) were perfused and post mortem dMRI were collected on a 4.7T Agilent pre-clinical MRI scanner using a 2D single spin-echo sequence with a single-line readout (voxel size 0.5 x 0.5 x 0.5 mm). Brains were sectioned parasagittally at 50 μm. Tracer paths were hand-drawn in Neurolucida in a 1-in-5 series of sections. Using each brainʼs fractional anisotropy (FA) images, probabilistic tractography was conducted using ProbtrackX2 from the FSL FDT toolbox seeding at the injection site. Histological data including section outline and grey-white matter boundaries were aligned with the dMRI FA image in MATLAB.Qualitatively, major streamline tracts aligned well with the labelled cortical projections from MST, LIP, and VIP, but not from V1 and V2 to V5/MT. Quantitatively, 2D spatial cross-correlation revealed considerable differences between the alignment of histological tracts and tractography streamlines in the anterior-posterior plane (mean drift: 1.9mm M127, 2.9mm M131) and dorsal-ventral plane (mean drift: 6.1mm M127, 7.0mm M131) in both brains.We applied Gaussian smoothing to tractography data and used receiver operating characteristic (ROC) curves to identify the overlap probability at different thresholds. We calculated the Area Under the Curve (AUC) and found reasonable overlap between tracer and tractography data (M127: AUC = 0.66, M131: AUC=0.80).Our results show that dMRI and tractography streamline can capture major aspects of specific white matter tract pathways, but major limitations still exist. The high curvature of tracts from V5/MT or towards V1 increases the likelihood of deviation from tracer data as distance from the seed point increases. Applying thresholds to tractography to include the top 99%, 95% or 90% of streamlines results in rapid data loss. Direct comparisons of high resolution dMRI data to underlying ground-truth histology can aid optimisation of data acquisition and tractography analysis to enhance the reliability and accuracy of non-invasive tracing of connections.

Characterization of social behavior in Shank2-deficient mice

Markus Fendt, Sevval Demirci, Aleksandra Gritskova, Evelyn Kahl, Ioanna-Maria Menegatou, Karthika Karthikabhavan Sudhan, Judith Kreutzmann

Shank2 is a large synaptic scaffold protein of then post-synaptic density involved in the organization of cytoskeleton-associated signaling complexes. Loss-of-function mutations of Shank2 in humans are associated with autism spectrum disorders, and Shank2-deficient mice exhibit autism-like behavior changes such as hyperactivity, increased anxiety, repetitive grooming, and abnormalities in social behavior. The aim of the present study is to characterize these changes in social behavior in more detail. Therefore, we submitted Shank2-deficient mice and their heterozygous and wildtype littermates to the following behavioral paradigms: (1) modified Crawley’s sociability test, (2) resident-intruder test, (3) exposure of male mice to sexually receptive female mice, (4) affective state discrimination, and (5) tube test for social dominance. Overall, we observed several changes in social behaviors that were related to Shank2 deficiency and could be interpreted as social deficits. However, some changes were sex-dependent, whereas some others were only observed in heterozygous mice. 

Modulation of positive emotional contagion in rats through playback of ultrasonic vocalizations: a longitudinal study

Emilie Bartsoen

Although Autism Spectrum Disorder (ASD) is characterized by deficits in complex social behavioral domains, such as empathy, in pre-clinical research the disorder is still largely modeled by simple behavioral tasks. To improve this restriction, we developed a novel test of emotional contagion (i.e., mimicking the affective state of a conspecific, also known as emotional empathy) in rats. Rats are highly social and communicate via ultrasonic vocalizations (USV). In aversive situations (e.g., exposure to predators), rats emit 22-kHz USV that presumably reflect a negative affective state. These USV serve as "alarm calls" and in response the rats freeze or hide. In appetitive situations (e.g., social play), rats emit 50-kHz USV that presumably reflect a positive affective state. They serve as "social contact calls" and elicit approach behavior in the receiving rat. Thus, 22-kHz and 50-kHz USV are thought to induce negative and positive affective states in the recipient, respectively. Our new emotional contagion protocol builds on the different affective properties of USV and combines them with the acoustic startle response (ASR) test. The ASR is a reflexive contraction of the body muscles in response to a loud noise burst and its intensity depends on the affective state of the animal - i.e., is strengthened in a negative affective state and but reduced in a positive affective state. Therefore, we conducted a longitudinal study in male (N=32) and female (N=32) Sprague-Dawley rats to test whether playback of both USV types could change the ASR in two opposite directions relative to their acoustic controls - i.e., enhanced and reduced by playback of 22-kHz and 50-kHz USV, respectively. All rats were tested as juveniles and as adults to examine age and sex effects. Our results show that playback of 50-kHz USV significantly reduced the ASR. This effect was consistently observed across all ages and sexes. Playback of 22-kHz USV did not significantly change the ASR compared to the acoustic control. However, a significant age effect was observed in male rats with increased ASR in response to playback of 22-kHz USV as adults versus juveniles. In summary, our new protocol was able to modulate positive emotional contagion in rats, distinguishing it from previous protocols that primarily focused on negative emotional contagion. Moreover, this protocol does not require learning because it uses ethologically relevant stimuli (i.e., USV). This will help us understand the complex psychological mechanisms involved in neurodevelopmental disorders, such as ASD.

Vasopressin release from the bed nucleus of stria terminalis to the lateral septum supports sociability and social aggression

Helena Bortolozzo & Félix Leroy, Instituto de Neurociencias, Alicante, Spain

The lateral septum (LS) is involved in a diverse set of motivated behaviors, including sociability and social aggression, which are also regulated by the release of the neuropeptide vasopressin (AVP) in LS. However, the sources of AVP release to LS remain unclear. We used anterograde and retrograde tracing techniques in Avp-Cre mice to determine the source of AVP to the LLS, revealing the bed nucleus of stria terminalis (BNST) as the major source of AVP+ neurons projecting to this region. Consistently, the BNST is also involved in sociability and social aggression. We then shower that chemogenetic silencing of AVP+ cells in the BNST impaired sociability and resident-intruder tests. Silencing the BNST AVP terminals to LS or genetic knock-down of Avp expression in BNST recapitulated the effect of chemogenetic silencing. Fiber-photometry recordings of AVP+ axon terminals from BNST to LS indicate that this projecting is active during sociability and social aggression. As AVP dysregulation is associated with social disorders, we characterized the behavioral deficits in the Shank3B+/- mouse model of autism spectrum disorder (ASD) and demonstrated that they display impaired sociability and aggression. We then showed that the BNST of Shank3B+/- mice contains less AVP+ neurons which leads to a decrease in AVP+ fiber density in anterior LS, suggesting that the dysregulation of the vasopressinergic system from BNST to LS is responsible for the abnormal social behaviors exhibited by the ASD mouse model. Overall, our work offers the first direct evidence of AVP source to LS, unraveling a circuit modulating distinct social behaviors and provides insights into the link between AVP and neurological disorders that impact social functioning. 

Impaired signaling of the autism candidate gene Reelin in somatostatin cortical neurons results in social communication alterations in mouse pups.

Livia Di Crescenzo1,2,3, Rani Moors2,3, Lynette Lim2,3, Markus Wöhr1,2,4,5

1KU Leuven, Laboratory of Biological Psychology, Social and Affective Neuroscience Research Group, Leuven, Belgium, 2KU Leuven, Leuven Brain Institute, Leuven, Belgium, 3VIB-KU Leuven Center for Brain & Disease Research, 4Philipps-University of Marburg, Faculty of Psychology, Experimental and Biological Psychology, Behavioral Neuroscience, Marburg, Germany, 5Philipps-University of Marburg, Center for Mind, Brain and Behavior, Marburg, Germany.

Autism Spectrum Disorder (ASD) is a class of neurodevelopmental disorders characterized by deficits in social communication. Even though Reelin (RELN) is known to be involved in ASD, its exact role remains largely unclear. We sought to evaluate the function of RELN in a cell-type specific manner to link inhibitory cortical circuit development to behavioral changes. Thus, we applied a behavioral approach to address social communication in mouse pups with a reduction or a lack of RELN specifically in somatostatin (SST+) inhibitory cortical neurons. The ultrasonic vocalizations (USV) emitted by mutant pups and controls of both sexes were repeatedly recorded in different behavioral tests. Furthermore, developmental milestones were also assessed during 4 timepoints of development. Protein analyses were carried out after the behavioral assays. Mutants and controls differed in USV emission, with mutants showing a peak of calls at postnatal day 6, while controls decreased their emission over time. Mutants also displayed shorter USV. Moreover, increased levels of a GABA biomarker have been found in the prefrontal cortex of mutant pups, suggesting that disrupting RELN signaling in SST+ neurons leads to an imbalance between excitatory and inhibitory transmission. Altogether, these results suggest that impairments in RELN expression in SST+ inhibitory cortical neurons may result in social communication alterations in mouse pups. 

Multisensory processing of social information in the medial amygdala

S. Bailey, D. Regester, J. Yin, Y. Isogai

Instinctive social behaviours such as mating, aggression, and parenting, are crucial to survival. However, it remains unclear how the brain interprets the wide range of social sensory stimuli that drive ethologically appropriate actions. In mice, which depend heavily on the vomeronasal pathway to identify conspecifics, the medial amygdala (MeA) is a strong candidate for coordinating such responses, since this area receives dense vomeronasal inputs. Previous studies have also shown that activation of genetically identified subpopulations in MeA are sufficient to drive various innate social behaviours, many of which are strongly associated to brain regions directly downstream of MeA. Using Neuropixel 2.0 probes, we record from MeA in head-fixed animals and present a range of volatile, non-volatile, and tactile stimuli derived from conspecifics. We find that the MeA neurons respond reliably to all three forms of stimulus modality, and stimulus identity can be decoded from population activity. Additionally, we observed a biphasic response profile to co-presentations of volatile and non-volatile cues. To identify the origin of the different phases of the response, we first eliminated sensory neurons from the main olfactory pathway. We found that these inputs are necessary for the early phase of biphasic responses, but play a minor role in decoding stimulus identity. We then evaluated how local circuit components contribute to sensory processing in MeA. Ablation of a unique interneuron population that receives inputs from vomeronasal and olfactory pathways caused a large depression in the late phase of biphasic dynamics and stimulus coding was markedly compromised. From these results we propose a disinhibitory circuit model in which local interneurons gate MeA neuron activity in a modality-specific manner. This mechanism could explain how the medial amygdala selectively integrates multimodal sensory inputs to flexibly coordinate the expression of different social behaviours.

Mathematical modeling of marmoset vocal accommodation 

Nikhil Phaniraj1,2,3*, Kaja Wierucka1,4, Judith M. Burkart1,2,5

1Institute of Evolutionary Anthropology, University of Zurich; Winterthurerstrasse 190, 8057 Zürich, Switzerland.2Neuroscience Center Zurich (ZNZ), University of Zurich and ETH Zurich; Winterthurerstrasse 190, 8057 Zürich, Switzerland.3Department of Biology, Indian Institute of Science Education and Research (IISER) Pune; Dr. Homi Bhabha Road, Pune 411008, India.4Behavioural Ecology and Sociobiology Unit, German Primate Center – Leibniz Institute for Primate Research, Kellnerweg 4, 37077 Göttingen, Germany.5Center for the Interdisciplinary Study of Language Evolution (ISLE), University of Zurich; Affolternstrasse 56, 8050 Zürich, Switzerland.*Corresponding author. Email: nikhil.phaniraj@uzh.ch

Vocal production learning (VPL) plays an important role during speech development in human infants and is vital for language. VPL in humans, however, is not restricted to infants. Adults continue to show socially influenced, but modest changes in speech in the form of social vocal accommodation (SVA). This adult form of VPL remains understudied and the complex structure of language creates a colossal challenge in tracking vocal changes during SVA. Consequently, animals with simpler vocal communication systems are powerful tools for understanding the mechanisms underlying SVA. In this study, we tracked acoustic changes in the vocalizations of adult common marmosets, a highly vocal primate species known to show SVA, for up to 85 days after pairing with a partner. We identified four properties of SVA in marmosets: (1) bidirectional vocal learning, (2) exponential decrease in the vocal distance between the paired individuals with time, (3) sensitivity to initial vocal distance and (4) dyadic acoustic feature synchrony during SVA. We then developed a mathematical model that showed all four properties of marmoset SVA to explain the observed temporal dynamics. The model suggests that marmosets match their vocalizations to a dynamic template that is constantly updated to account for the changes in their partners’ vocalizations. The model provides crucial insights into the mechanisms underlying SVA in adult animals and how they might differ from those underlying VPL in infants.

Gray matter ontogenetic trajectories and socio-cognitive development in the prosocial, cooperatively breeding, common marmoset

Paola Cerrito1,2, Judith M. Burkart1,3*

1 Department of Evolutionary Anthropology, University of Zurich, Zürich, Switzerland2 Collegium Helveticum, ETH Zürich, Schmelzbergstrasse 25, Zürich, 8092, Switzerland3Center for the Interdisciplinary Study of Language Evolution (ISLE), University of Zurich, Zürich, Switzerland

Brain ontogeny in primates, and especially in humans, is experience-dependent: it is affected by the stimuli received during a critical period. In early development, these stimuli differ substantially between independently and cooperatively breeding species. In cooperative breeders, starting right after birth, infants interact with multiple caregivers and therefore must adapt to a richer and more varied social environment. Here, we examine the region-specific gray matter ontogenetic trajectories of the cooperatively breeding common marmoset (Callithirx jacchus) and relate them to behavioral and developmental milestones. We target brain regions that are significantly more involved than others when observing social interactions and find that: (i) these regions share similar developmental trajecotires; (ii) these regions attain their maximum volume right after peak provisioning by group members; (iii) in these regions the volumetric reduction to adult size coincides with the period of frequent negotiations between infants and caregivers over food, the arrival of the next set of siblings, and the change of role from being a recipient of care to becoming a helper. Similarly to humans, gray matter volumetric reduction is not fully completed when the first reproductive event occurs. Overall, we find that the ontogenetic trajectory of brain areas implicated in the evaluation of social interactions coincides with fundamental social milestones and developmental tasks in marmosets and progresses into early adulthood. The rich social environment in which infants of cooperative breeders are raised during a critical period of brain ontogeny appears fundamental for the emergence of the particularly strong prosociality and socio-cognitive skills of marmosets. Since humans are also cooperative breeders, our findings have significant implications for the evolution of human social cognition.

Rapid and exact facial mimicry in infant chimpanzees 

Sarah Salphati1 , Derry Taylor , Kenna Valles3, and Marina Davila-Ross1

Affilitations: 1 Psychology Department, University of Portsmouth, King Henry Building, Portsmouth 2 Ape Social Mind Lab, Institut of Cognitive Science Marc Jeannerod, CNRS, Lyon, France3 Royal Dick School of Veterinary Studies, University of Edinburgh, Easter Bush Campus, Edinburgh

From young ages onward, humans are known to mimic the facial expressions of others. The mimicking of facial expressions, particularly when performed rapidly (i.e., within one second) and exactly (i.e., matching of the same facial variant), is thought to serve important functions, linked to emotional congruence and enhanced cohesion within a social group. This study tested for rapid and exact mimicry in chimpanzees (Pan troglodytes) under the age of five (N = 24) during spontaneous, dyadic play. We examined two variants of open-mouth expressions (OMFs), i.e., without upper teeth exposure (NoUT) and with upper teeth exposure (UT). Results indicated that significantly more infants produced congruent (i.e., OMF within one second of an OMF) than non-congruent facial expressions (i.e., no OMF within one second of an OMF). It was also found that infants exactly replicated one OMF variant (NoUT) but not the other (UT). These findings provide the first evidence that rapid and exact mimicking of open-mouth expressions is already present at a very young age in chimpanzees. Such facial behaviours may thus be deeply rooted in this taxon, and likely playing a very important role in their everyday social interactions. 

Behavioral mechanisms and premotor cortex representations of dyadic coordination in transparent games

Igor Kagan, Sebastian Moeller, Zahra Yousefi Darani, Stefan Treue, Alexander Gail

Many real-world social interactions unfold in continuous time under conditions of mutual action visibility. I will present our recent work on dynamic strategic coordination underlying such interactions, utilizing a novel face-to-face setup based on a two-sided touch-sensitive, transparent display. In the first experiment, we studied the behavior of macaque and human dyads in a “transparent” version of the classical “Bach-or-Stravinsky” decision game, which rewards coordinated choices but also imposes an inherent conflict. While humans predominantly adopted dynamic pro-social turn-taking to equalize payoffs, macaques converged on simpler, static coordination. After training with a human confederate, macaques learned to follow and coordinate dynamically but exhibited competitive turn-taking when paired together. In the second experiment, two trained macaques, implanted with 160-channel recording arrays in the dorsal and ventral premotor cortex, made spatial reaching decisions before, concurrently with, or after their partner’s action (a dyadic context), or without a partner (a solo context). Single neurons and population activity represented predicted and observed actions of a partner, and integrated this information with the encoding of the agent’s own goals, expected value, and choices. These results demonstrate how action visibility promotes the emergence and maintenance of coordination, against the backdrop of varying social attitudes and motivations in both species, and highlight the contribution of the premotor cortex to neuronal computations during dynamic strategic interactions.

Confidence over competence: Perceptual decision-making during dyadic interactions in a continuous perceptual report

F. Schneider1, A. Calapai1, A. Gail2,4, I. Kagan3, S. Treue1,4

1 Cognitive Neuroscience Laboratory, German Primate Center – Leibniz-Institute for Primate Research, Goettingen, Germany2 Sensorimotor Group, German Primate Center, Goettingen, Germany3 Decision and Awareness Group, German Primate Center, Goettingen, Germany4 Faculty of Biology and Psychology, Georg-August University, Goettingen, Germany

Perceptual decision-making is a dynamic process in which individuals collect, evaluate, and integrate sensory evidence to produce adequate behavior. Perceptual confidence plays a key role in this process. However, the majority of perceptual decision-making paradigms do not provide a readout of confidence.We developed a continuous perceptual report (CPR) paradigm to measure perceptual confidence in real-time. With this approach we assessed (i) the influence of sensory evidence strength on individuals’ decision-making and (ii) how real-time access to perceptual responses of a partner influences decision-making. We collected psychophysical data from human participants in two conditions: alone (solo) and together with a partner (dyadic). Dyadic conditions could be real, with two participants playing simultaneously; or simulated, with a participant (who is led to believe to be playing with another participant) playing alongside a reliably accurate computer agent. In the CPR task, a random-dot pattern (RDP), changing frequently in motion direction and coherence level within a stationary circular aperture, is predictive of the location of briefly appearing reward targets. Subjects control a cursor with a joystick and are instructed to ‘collect’ targets by aligning the cursor to the perceived motion direction. The cursor size is coupled to the joystick’s eccentricity, such that higher eccentricity - indicative of higher confidence - results in a smaller cursor. When a target is collected both accuracy and confidence are taken into account to determine the reward score. This results in peri-decision wagering, as accurate and confident responses yield high scores; less accurate and low confidence responses, or accurate and low confident responses, both yield low score; and inaccurate responses are always misses. While in the solo condition, subjects see only their own cursor, in dyadic settings both cursors and scores are visible to both participants at all times.We show that performance and perceptual confidence are not only determined by task difficulty but also by the social context. During human-human co-action, most subjects changed significantly in their confidence output but not in task competence measures. Within individual dyads, players converged in confidence and accuracy. In addition, control experiments with a simulated computer agent demonstrate reliable integration of accurate social cues, suggesting long-term reliability as a driver of social evidence integration. Together, these results indicate that both perceptual and meta-cognitive processes are modulated by the availability of social information, with robust effects in the confidence domain.

Understanding vigilance behaviour in common marmosets

Rahel K. Brügger1, Nikhil Phaniraj1, 2, 3, Judith M. Burkart1, 2, 3 

1 Institute of Evolutionary Anthropology, University of Zurich, Switzerland2 Neuroscience Center Zurich, University of Zurich and ETH Zurich, Switzerland 3 Center for the Interdisciplinary Study of Language Evolution (ISLE), University of Zurich, Switzerland 

A lot of the understanding of prosocial behaviours in animals stems from experiments where individuals are subjected to tasks in a very controlled environment to quantify their willingness to cooperate. Such tasks fall short to estimate how much cognitive flexibility animals can exhibit in more naturalistic cooperative interactions. Common marmosets are an ideal model species to study prosocial behaviours as their cooperative breeding system necessitates a high willingness to coordinate helping behaviour in the domain of infant care (i.e., food sharing and carrying) but less is known about vigilance behaviour. Here we present data on vigilance behaviour in captive marmoset individuals (N = 14) in a feeding context, where being vigilant and feeding is mutually exclusive. We show that pairs of individuals minimize the time when no one is vigilant, and in particular increase their vigilance level when pair mates are feeding. This results in an anti-phase (in other words turn-taking) pattern of feeding and being vigilant. Moreover, we were interested in how much control over this emerging anti-phase vigilance behaviour marmosets truly exhibit. We therefore modelled pairs as coupled oscillators and show that coupling is not fixed. Intriguingly, the marmosets worked harder to achieve anti-phase synchrony (higher coupling strength) when the initial state of the pair was similar (i.e., both were feeding, or both were vigilant). Achieving turn-taking also had benefits because individual feeding bouts were longer when in anti-phase with the partner. We provide evidence for coordination of cooperative behaviour in a naturalistic context and a mathematical framework to investigate cognitive aspects of coordinated behaviours more generally. 

The effect of reward value on the performance of long-tailed macaques (Macaca fascicularis) in a delay of gratification exchange task

Judit J. Stolla1,2, Julia Fischer1,2,3 & Stefanie Keupp1,2,3

1 German Primate Center - Leibniz Institute for Primate Research, Cognitive Ethology Laboratory, Kellnerweg 4, 37077 Göttingen, Germany

2 Georg-August-Universität Göttingen, Johann-Friedrich-Blumenbach Institute, Department for Primate Cognition, Kellnerweg 4, 37077 Göttingen, Germany

3 Leibniz ScienceCampus, German Primate Center - Leibniz Institute for Primate Research, Kellnerweg 4, 37077 Göttingen, Germany

In a current call for data collection of a large-scale collaboration project (ManyPrimates), researchers worldwide collect data to compare the ability to delay gratification in different primate species. We contributed data from long-tailed macaques (Macaca fascicularis) and found that they rarely exchanged the provided food item for more food later. However, we had the impression that the protocol might not adequately reflect the abilities of the study subjects. More specifically, we suspected that possession of a high value food item interfered with engagement in any participation in a food exchange task or delay of gratification paradigm. To disentangle this potential mental block from poor delay of gratification skills, we tested six long-tailed macaques in two conditions, in which we assessed the effect of the value of an exchange item and the relative value difference on the frequency of exchanges. Subjects received either a high or low value food item, which could be exchanged for three high value food items. The monkeys exchanged low value food items more often than high value food items across three delay periods. Furthermore, the probability for an exchange decreased with increasing delay period. Reducing the value of the exchange item resulted in long-tailed macaques showing considerably better abilities to delay gratification in an exchange task. These findings indicate that being in possession of a high value item played a substantial role in the low performance of these monkeys in the original delay of gratification exchange protocol.

Can increased foraging capability make a baboon more popular? A manipulative field experiment in the tolerant multi-level society of Guinea baboons

William O’Hearn, Jörg Beckmann, Lorenzo von Fersen, Carolin Niederbremer, Roger Mundry, Federico Dal Pesco, and Julia Fischer

Successfully navigating a group’s social environment means making adaptive partner choices, which is facilitated by the ability to evaluate the social ties, traits, or capabilities of other group members. Much is known about non-human primates’ knowledge of third-party kin, dominance, and social relationships. However, less is understood about how individuals evaluate others’ capabilities. Our project investigates whether Guinea baboons in one captive and two wild groups recognise the foraging capability of group members, and whether knowledge of conspecifics’ capabilities affect their choice of social partners. In our study we artificially increase the foraging capability of one group member using an apparatus only the chosen individual – the specialist – can operate. We measure the specialist’s social interactions before, during, and after the period of apparatus presentations to determine if other group members alter their treatment of the specialist in response to their novel foraging capability. We also collect association data from the whole group across the study period to see if the newly capable specialist becomes more central in their social network. My poster will present the findings from our study, which breaks new ground by testing assessment of foraging capability in a socially tolerant multi-level society that is minimally structured by kinship or dominance rank.

Investigating behavioral and neural mechanisms underlying helping behavior in mice

Esmeralda Tafani, Charitha Omprakash, Moises dos Santos Correa, Ada Braun, Anna Agafonova, Melissa Lowitsch, Anne Albrecht, Pavol Bauer & Sanja Mikulovic

A growing body of research compellingly illustrates the manifestation of empathy and prosocial behaviors in rodents. However, our comprehension of the specific behavioral variables, brain regions, and circuits governing these behaviors remains limited. To address this gap, we conducted a helping behavior experiment in mice, exposing one individual to mild and high-stress conditions. Notably, heightened stress more significantly influenced helping, with female mice exhibiting a reduced latency to assist the stressed individual. Our subsequent inquiry addressed the emotional arousal of the helper. When exposed to the predator odor of a hunting cat, we observed a delay in helping behavior, particularly in females. Given the hippocampus's role in encoding cognitive and emotional processes along its dorsoventral axis, our investigation focused on the involvement of the dorsal hippocampus (dHPC) in helping behavior. Through chemogenetic inhibition of dHPC, we observed a remarkable decrease in helping behavior over time. Brain-wide CFos quantification revealed that inhibiting dHPC led to a reduced number of CFos+ cells in the basolateral amygdala and ventral hippocampus (vHPC). To further elucidate the neural mechanisms, we employed One-Photon Calcium imaging using miniscopes during the helping behavior. Utilizing decoder analysis, we identified the decodability of various displayed behaviors in mice by dHPC circuits, including door interactions to aid individuals in need. These findings suggest that dHPC circuits play a causal role in decoding prosocial behavior.