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Linking Social Cognition to Learning and Memory

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Leblanc, Heloise, Ramirez, Steve·2020·The Journal of Neuroscience

DOI 10.1523/jneurosci.1280-20.2020PMC PMC7659449

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Abstract

Many mammals have evolved to be social creatures. In humans, the ability to learn from others' experiences is essential to survival; and from an early age, individuals are surrounded by a social environment that helps them develop a variety of skills, such as walking, talking, and avoiding danger. Similarly, in rodents, behaviors, such as food preference, exploration of novel contexts, and social approach, can be learned through social interaction. Social encounters facilitate new learning and help modify preexisting memories throughout the lifespan of an organism. Moreover, social encounters can help buffer stress or the effects of negative memories, as well as extinguish maladaptive behaviors. Given the importance of such interactions, there has been increasing work studying social learning and applying its concepts in a wide range of fields, including psychotherapy and medical sociology. The process of social learning, including its neural and behavioral mechanisms, has also been a rapidly growing field of interest in neuroscience. However, the term “social learning” has been loosely applied to a variety of psychological phenomena, often without clear definition or delineations. Therefore, this review gives a definition for specific aspects of social learning, provides an overview of previous work at the circuit, systems, and behavioral levels, and finally, introduces new findings on the social modulation of learning. We contextualize such social processes in the brain both through the role of the hippocampus and its capacity to process “social engrams” as well as through the brainwide realization of social experiences. With the integration of new technologies, such as optogenetics, chemogenetics, and calcium imaging, manipulating social engrams will likely offer a novel therapeutic target to enhance the positive buffering effects of social experiences or to inhibit fear-inducing social stimuli in models of anxiety and post-traumatic stress disorder.

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Vasopressin 1b Receptor Knock-Out Impairs Memory for Temporal Order
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The hippocampus and motivation.
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Cerebellar Contribution to Spatial Event Processing: Morris Water Maze and T‐maze
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Spatial and Temporal Locomotor Learning in Mouse Cerebellum
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Long-Term Social Recognition Memory Is Mediated by Oxytocin-Dependent Synaptic Plasticity in the Medial Amygdala
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Observational Learning and Social Facilitation in the Rat
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Neural Circuits for Social Cognition: Implications for Autism
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Autonomic brainstem nuclei are linked to the hippocampus
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Social Memory and the Role of the Hippocampal CA2 Region
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Sex differences in the neurobiology of fear conditioning and extinction: a preliminary fMRI study of shared sex differences with stress-arousal circuitry
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Two types of social buffering differentially mitigate conditioned fear responses
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Comparative studies of social buffering: A consideration of approaches, terminology, and pitfalls
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Dynamics of social representation in the mouse prefrontal cortex
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Social learning in humans and other animals
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Aging and sex influence the anatomy of the rat anterior cingulate cortex
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A role for CA3 in social recognition memory
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Microglial P2Y12 receptor regulates ventral hippocampal CA1 neuronal excitability and innate fear in mice
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Oxytocin, vasopressin, and the motivational forces that drive social behaviors
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Fear conditioning by-proxy: Social transmission of fear during memory retrieval
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A familiar conspecific is more effective than an unfamiliar conspecific for social buffering of conditioned fear responses in male rats
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Evolutionary functions of early social modulation of hypothalamic–pituitary–adrenal axis development in humans
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The Long Journey of Pontine Nuclei Neurons: From Rhombic Lip to Cortico-Ponto-Cerebellar Circuitry
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A hippocampus to prefrontal cortex neural pathway inhibits food motivation through glucagon-like peptide-1 signaling
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Representation of actions in rats: The role of cerebellum in learning spatial performances by observation
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Hippocampus ghrelin signaling mediates appetite through lateral hypothalamic orexin pathways
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Behavioral and mechanistic insight into rodent empathy
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Effect of Visuospatial Attention on the Sensorimotor Gating System
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Stress-induced hyperthermia as a putative anxiety model
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Oxytocin in learning and addiction: From early discoveries to the present
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The topological anatomy of the hippocampus: A clue to its function
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Convergence of entorhinal and CA3 inputs onto pyramidal neurons and interneurons in hippocampal area CA1—An anatomical study in the rat
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Oxytocin Activation of Maternal Behavior in the Rata
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Neural Basis of Observational Fear Learning: A Potential Model of Affective Empathy
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Little and often: Ingestive behavior patterns following hippocampal lesions in rats.
Clifton, P. G., Vickers, S. P., & Somerville, E. M. (1998) · Behavioral Neuroscience · doi:10.1037//0735-7044.112.3.502 · Cited by 100
Social memories in rodents: Methods, mechanisms and modulation by stress
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Social memory engram in the hippocampus
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Alarm pheromone enhances stress-induced hyperthermia in rats
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An intra-amygdala circuit specifically regulates social fear learning
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“…and fear conditioning by proxy In contrast to mice, rats do not need prior direct fear conditioning experience to acquire or recall a social engram formed when observing a demonstrator rat undergo contextual or auditorycued fear conditioning (Yusufishaq and Rosenkranz, 2013; Twining et al., 2017).”
Background
Intelligent Social Learning.
Conte, R., & Paolucci, M. (2001) · Cited by 92
Consolidation of memory
Nadel, L., & Bohbot, V. D. (2001) · Hippocampus · doi:10.1002/1098-1063(2001)11:1 · Cited by 92
Little and often: Ingestive behavior patterns following hippocampal lesions in rats.
Clifton, P. G., Vickers, S. P., & Somerville, E. M. (1998) · Behavioral Neuroscience · doi:10.1037/0735-7044.112.3.502 · Cited by 92
Empathic Fear Responses in Mice Are Triggered by Recognition of a Shared Experience
Sanders, J., Mayford, M., & Jeste, D. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074609 · Cited by 90 · cited 7×
“…of prior experience with unconditioned stimuli for an observer to acquire a fear association by observation of a conspecific (Chen et al., 2009; Bruchey et al., 2010; Jeon et al., 2010; E. J. Kim et al., 2010; Atsak et al., 2011; Pereira et al., 2012; Sanders et al., 2013; Allsop et al., 2018).”
BackgroundMethodResultInfluential
Stress-induced hyperthermia in mice: Hormonal correlates
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The Hippocampus as a Cognitive Map … of Social Space
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Silence resulting from the cessation of movement signals danger
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Role of oxytocin receptors in modulation of fear by social memory
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The Cerebellum in Social Cognition
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Social modeling of conditioned fear in mice by non-fearful conspecifics
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Hippocampal Area CA2: An Overlooked but Promising Therapeutic Target
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Social transmission of Pavlovian fear: fear-conditioning by-proxy in related female rats
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Influence of fear conditioning on elicited ponto-geniculo-occipital waves and rapid eye movement sleep.
Sanford, L., Silvestri, A. J., Ross, R. J., & Morrison, A. R. (2001) · PubMed · Cited by 81
Dominance status predicts social fear transmission in laboratory rats
Jones, C. E., & Monfils, M.-H. (2016) · Animal Cognition · doi:10.1007/s10071-016-1013-2 · Cited by 81
The hippocampus and reward: Effects of hippocampal lesions on progressive-ratio responding.
Schmelzeis, M. C., & Mittleman, G. (1996) · Behavioral Neuroscience · doi:10.1037/0735-7044.110.5.1049 · Cited by 81
Post-weaning social isolation impairs observational fear conditioning
Yusufishaq, S., & Rosenkranz, J. A. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.12.050 · Cited by 80
Acute psychosocial stress effects on memory performance: Relevance of age and sex
Hidalgo, V., Pulopulos, M. M., & Salvador, A. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.11.013 · Cited by 80
Memory systems 2018 – Towards a new paradigm
Ferbinteanu, J. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.11.005 · Cited by 75
Social dominance hierarchy type and rank contribute to phenotypic variation within cages of laboratory mice
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Hippocampal c-fos is necessary for long-term memory of a socially transmitted food preference
Countryman, R. A., Kaban, N. L., & Colombo, P. J. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.07.005 · Cited by 73
Social Circuits: Peptidergic Regulation of Mammalian Social Behavior
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Social Learning in Animals Sex Differences and Neurobiological Analysis
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Leptin-Induced Spine Formation Requires TrpC Channels and the CaM Kinase Cascade in the Hippocampus
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Combined Lesions of Hippocampus and Subiculum Do Not Produce Deficits in a Nonspatial Social Olfactory Memory Task
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A Principle for Describing and Verifying Brain Mechanisms Using Ongoing Activity
Eriksson, D. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00001 · Cited by 67
Sleep deprivation impairs contextual fear conditioning and attenuates subsequent behavioural, endocrine and neuronal responses
Hagewoud, R., BULTSMA, L. J., Barf, R. P., Koolhaas, J. M., & Meerlo, P. (2010) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2010.00895.x · Cited by 65
From Engrams to Pathologies of the Brain
Denny, C. A., Lebois, E. P., & Ramirez, S. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00023 · Cited by 65
Self-citation
Rodent models for studying empathy
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Fear conditioning increases NREM sleep.
Hellman, K., & Abel, T. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.2.310 · Cited by 62
Excitotoxic lesions of the hippocampus disrupt runway but not consummatory contrast
Flaherty, C. F., Coppotelli, C., Hsu, D., & Otto, T. A. (1998) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00138-1 · Cited by 61
Sex Differences in Remote Contextual Fear Generalization in Mice
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Contextual Fear Extinction Ameliorates Sleep Disturbances Found Following Fear Conditioning in Rats
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Hippocampal area CA2: an emerging modulatory gateway in the hippocampal circuit
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Biological mechanisms for observational learning
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Role of the main olfactory system in recognition between individual spiny mice
Matochik, J. A. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90073-x · Cited by 59
The neural pathway underlying social buffering of conditioned fear responses in male rats
Kiyokawa, Y., Wakabayashi, Y., Takeuchi, Y., & Mori, Y. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08257.x · Cited by 58
Selective lesions of basal forebrain cholinergic neurons produce anterograde and retrograde deficits in a social transmission of food preference task in rats
Vale-Martı́nez, A., Baxter, M. G., & Eichenbaum, H. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02153.x · Cited by 58
Observation of Distressed Conspecific as a Model of Emotional Trauma Generates Silent Synapses in the Prefrontal-Amygdala Pathway and Enhances Fear Learning, but Ketamine Abolishes those Effects
Ito, W., Erişir, A., & Morozov, A. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.100 · Cited by 56
Insights from social transmission of information in rodents
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Regulation of Memory Function by Feeding-Relevant Biological Systems: Following the Breadcrumbs to the Hippocampus
Suarez, A. N., Noble, E. E., & Kanoski, S. E. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00101 · Cited by 55
Optogenetic reactivation of prefrontal social neural ensembles mimics social buffering of fear
Gutzeit, V. A., Ahuna, K., Santos, T. L., Cunningham, A. M., Rooney, M. S., Zamora, A., Denny, C. A., & Donaldson, Z. R. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0631-1 · Cited by 55
Hippocampus ghrelin receptor signaling promotes socially-mediated learned food preference
Hsu, T. M., Noble, E. E., Reiner, D. J., Liu, C. M., Suarez, A. N., Konanur, V., Hayes, M. R., & Kanoski, S. E. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.11.039 · Cited by 54
A Mouse Model for Observational Fear Learning and the Empathetic Response
Jeon, D., & Shin, H. (2011) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0827s57 · Cited by 52
Rapid forgetting of social transmission of food preferences in aged rats: Relationship to hippocampal CREB activationPreprint
Countryman, R. A., & Gold, P. E. (2007) · Learning & Memory · doi:10.1101/lm.524907 · Cited by 51
Social buffering enhances extinction of conditioned fear responses in male rats
Mikami, K., Kiyokawa, Y., Takeuchi, Y., & Mori, Y. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.05.001 · Cited by 51
Proximodistal Organization of the CA2 Hippocampal Area
Fernández‐Lamo, I., Gómez-Domínguez, D., Sánchez-Aguilera, A., Oliva, A., Morales, A. V., Valero, M., Cid, E., Berényi, A., & de la Prida, L. M. (2018) · Cell Reports · doi:10.1016/j.celrep.2019.01.060 · Cited by 51
Social biology of rodents
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Acetylcholine in the orbitofrontal cortex is necessary for the acquisition of a socially transmitted food preferencePreprint
Ross, R. S., McGaughy, J. A., & Eichenbaum, H. (2005) · Learning & Memory · doi:10.1101/lm.91605 · Cited by 46
Rat Strain Differences in Freezing and Sleep Alterations Associated with Contextual Fear
Tang, X., Yang, L., & Sanford, L. D. (2005) · SLEEP · doi:10.1093/sleep/28.10.1235 · Cited by 46
Similar levels of emotional contagion in male and female rats
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Temporary basolateral amygdala lesions disrupt acquisition of socially transmitted food preferences in ratsPreprint
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22 kHz and 55 kHz ultrasonic vocalizations differentially influence neural and behavioral outcomes: Implications for modeling anxiety via auditory stimuli in the rat
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Time-courses of Fos expression in rat hippocampus and neocortex following acquisition and recall of a socially transmitted food preference
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Muscarinic receptor blockade in ventral hippocampus and prelimbic cortex impairs memory for socially transmitted food preference
Márquez, A. C., Vale-Martı́nez, A., Guillazo‐Blanch, G., & Martí‐Nicolovius, M. (2008) · Hippocampus · doi:10.1002/hipo.20530 · Cited by 41
The breeding strategy of female jumbo squid Dosidicus gigas: energy acquisition and allocation
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Oxytocin and the Social Brain
Fineberg, S. K., & Ross, D. A. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.11.004 · Cited by 40
Observation and discrimination learning in the rat: Effects of stimulus substitution
Kohn, B. (1976) · Learning and Motivation · doi:10.1016/0023-9690(76)90038-2 · Cited by 39
The Role of the Medial Prefrontal Cortex in Regulating Social Familiarity-Induced Anxiolysis
Lungwitz, E. A., Stuber, G. D., Johnson, P. L., Dietrich, A. D., Schartz, N. D., Hanrahan, B., Shekhar, A., & Truitt, W. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.302 · Cited by 39
Anterograde and Retrograde Amnesia After Lesions to Frontal Cortex in Rats
Winocur, G., & Moscovitch, M. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-21-09611.1999 · Cited by 39
Threat of shock and aversive inhibition: Induced anxiety modulates Pavlovian-instrumental interactions.
Mkrtchian, A., Roiser, J. P., & Robinson, O. J. (2017) · Journal of Experimental Psychology General · doi:10.1037/xge0000363 · Cited by 38
Involvement of rat posterior prelimbic and cingulate area 2 in vocalization control
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Phosphorylation sites of microtubule-associated protein 1B (MAP 1B) are involved in axon growth and regeneration
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Functional anomalies in healthy individuals with a first degree family history of major depressive disorder
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See all 69

Authors: Leblanc, H., & Ramirez, S.
Affiliations: Boston University (US)
ORCID: Ramirez, Steve
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2020-11-11
Volume: 40
Issue: 46
Pages: 8782-8798
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.1280-20.2020
PMC: PMC7659449
OpenAlex: W3101659541
Cited by: 69
References: 226
Citations by year: 2026: 6 · 2025: 20 · 2024: 18 · 2023: 7 · 2022: 14 · 2021: 4
FWCI: 0.84
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 181 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: HHS | NIH | NIH Office of the Director
McKnight Endowment Fund for Neuroscience
Brain and Behavior Research Foundation
Ludwig Family Foundation
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: social learning, social cognition, hippocampus, memory modulation, social buffering, anxiety, post-traumatic stress disorder, social interaction
MeSH terms: Social Cognition, Animals, Humans, Learning, Memory, Social Behavior, Optogenetics

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Linking Social Cognition to Learning and Memory

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