Social behavior in prepubertal neurexin 1α deficient rats: A model of neurodevelopmental disorders.
Open accessAbstract
Loss-of-function mutations in the synaptic protein neurexin1α (NRXN1α) are associated with several neurodevelopmental disorders, including autism spectrum disorder (ASD), schizophrenia, and attention-deficit hyperactivity disorder (ADHD), and many of these disorders are defined by core deficits in social cognition. Mouse models of Nrxn1α deficiency are not amenable to studying aspects of social cognition because, in general, mice do not engage in complex social interactions such as social play or prosocial helping behaviors. Rats, on the contrary, engage in these complex, well-characterized social behaviors. Using the Nrxn1tm1Sage Sprague Dawley rat, we tested a range of cognitive and social behaviors in juveniles with haplo- or biallelic Nrxn1α mutation. We found a deficit in ultrasonic vocalizations (USVs) of male and female neonatal rats with Nrxn1α deficiency. A male-specific deficit in social play was observed in Nrxn1α-deficient juveniles, although sociability and social discrimination were unaltered. Nurturing behavior induced by exposure to pups was enhanced in male and female juveniles with biallelic Nrxn1α mutation. Performance in tasks of prosocial helping behavior and food retrieval indicated severe deficits in learning and cognition in juveniles with biallelic Nrxn1α mutation, and a less severe deficit in haploinsufficient rats, although Pavlovian learning was altered only in haploinsufficient males. We also observed a male-specific increase in mobility and object investigation in juveniles with complete Nrxn1α deficiency. Together, these observations more fully characterize the Nrxn1tm1Sage Sprague Dawley rat as a model for Nrxn1α-related neurodevelopmental disorders, and support a rationale for the juvenile rat as a more appropriate model for disorders that involve core deficits in complex social behaviors. (PsycInfo Database Record (c) 2021 APA, all rights reserved).
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Previous studies with nrxn1-deficient rats have shown sex-specific deficits in ultrasonic vocalizations and social play, but unaffected sociability and social discrimination.
“sex-specific deficits in ultrasonic vocalizations and social play, but unaffected sociability and social discrimination (Kight et al. 2021).”
From Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia (2025) · cites this paper as Kight et al. 2021
The Abstract reports reduced ultrasonic vocalizations in both male and female neonatal rats, but a male-specific deficit in juvenile social play. It also reports unaltered sociability and social discrimination. Thus, the claim is supported except for describing the vocalization deficit as sex-specific. (LLM, conf=0.90)
Experimental — accuracy not yet measuredThe Kight et al. (2021) study scored behaviour of individual rats, averaged over 4 days of testing in a non-habituated setting.
“That is, the Kight et al. (2021) study scored behaviour of individual rats, averaged over 4 days of testing in a non-habituated setting.”
From Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia (2025) · cites this paper as Kight et al. (2021)
The Materials and Methods section (Juvenile Rough-and-Tumble Play Behavior; page unavailable) says videos were scored for each rat and individual scores were averaged across four days. It does not describe the setting as non-habituated; the pairs were allowed to acclimate in the enclosure for two minutes before recording. (LLM, conf=0.85)
Experimental — accuracy not yet measurednrxn1-KO rats show marked locomotor hyperactivity.
“we also observed marked locomotor hyperactivity in the nrxn1-KO rats, consistent with previous studies (Esclassan et al. 2015; Kight et al. 2021).”
From Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia (2025) · cites this paper as Kight et al. 2021
The Results section (‘KO Males Show Increased Locomotion in the Open Field’) reports significantly greater distance traveled by KO males than by wild-type and heterozygous males. It also reports no locomotor effect in females, so the unqualified claim about KO rats overgeneralizes a male-specific open-field finding. (LLM, conf=0.90)
Experimental — accuracy not yet measurednrxn1-KO rats were hyperactive in the amphetamine experiment.
“In this experiment, nrxn1-KO rats were hyperactive, as was found previously (Esclassan et al. 2015; Kight et al. 2021)”
From Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia (2025) · cites this paper as Kight et al. 2021
The Results section, “SD-Nrxn1tm1sage KO Males Show Increased Locomotion in the Open Field” (page unavailable), supports the citation’s point that KO rats had previously shown hyperactivity—but only in prepubertal males. It reports no locomotor effect in females. The cited study tested open-field locomotion, not hyperactivity in an amphetamine experiment; the citing sentence describes that experiment as its own. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe strong increase in play behaviour in the nrxn1-KO rats in this study is in contrast to the decrease in play found previously by Kight et al. (2021).
“The strong increase in play behaviour in the nrxn1-KO rats in our study is in contrast to the decrease in play found previously by Kight et al. (2021).”
From Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia (2025) · cites this paper as Kight et al. (2021)
Important procedural differences between this study and Kight et al. (2021) may explain the discrepancy in results.
“there are also important procedural differences, which may explain the discrepancy in the obtained results.”
From Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia (2025) · cites this paper as Kight et al. (2021)
The profound hyperactivity of the nrxn1-KO rats in a novel environment may have interfered with the expression of social play in the Kight study.
“In addition, the profound hyperactivity of the nrxn1-KO rats in a novel environment (Esclassan et al. 2015; Kight et al. 2021; present study) may have interfered with the expression of social play in the Kight study”
From Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia (2025) · cites this paper as Kight et al. 2021
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Characterization of juvenile play in rats: importance of sex of self and sex of partner
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Self-citationEyeblink conditioning deficits indicate timing and cerebellar abnormalities in schizophrenia
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Antenatal origins of individual differences in heart rate
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Cerebellar functional abnormalities inSchizophrenia are suggested by classical eyeblink conditioning
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Self-citationHotspots of Large Rare Deletions in the Human Genome
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Important Contribution of α-Neurexins to Ca2+-Triggered Exocytosis of Secretory Granules
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Phenotypic characterization of nonsocial behavioral impairment in neurexin 1α knockout rats.
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Autism-Related Variation in Reciprocal Social Behavior: A Longitudinal Study
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Self-citationSex-Dependent Novelty Response in Neurexin-1α Mutant Mice
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Lessons from helping behavior in rats
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Molecular mechanism of parallel fiber-Purkinje cell synapse formation
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Developmental origins of sex differences in the neural circuitry of play
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Self-citationAbnormal empathy-like pro-social behaviour in the valproic acid model of autism spectrum disorder
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Neurexin regulates nighttime sleep by modulating synaptic transmission
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Self-citationPredator odor exposure of rat pups has opposite effects on play by juvenile males and females
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Self-citationCharacterization of speech and language phenotype in children with NRXN1 deletions
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The neurobiology of social play behaviour: Past, present and future
Achterberg, E. J. M., & Vanderschuren, L. J. M. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105319 · Cited by 56 · see citing works
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Self-citationBridging the translational gap: what can synaptopathies tell us about autism?
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Developmental exposure to the Fox River PCB mixture modulates behavior in juvenile mice
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Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia
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“Alongside the increases in social play behaviour, we also observed marked locomotor hyperactivity in the nrxn1-KO rats, consistent with previous studies (Esclassan et al. 2015; Kight et al. 2021).”
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Alpha-neurexins in health and disease
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An Empirical Study on the Motivation of Helping Behavior in RatsPreprint
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Roles of synaptic cell adhesion molecules in the neuromodulatory systems
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Age-dependent deficits of auditory brainstem responses in juvenile Neurexin1α knockout rats
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Fitzgerald, J., Molloy, C. J., Dinneen, T. J., Feerick, N., O’Sullivan, M., O’Conaill, R., Al-Shehhi, M., Reilly, R. B., Lynch, S. A., Heron, E. A., et al. (2025) · Journal of Neurodevelopmental Disorders · doi:10.1186/s11689-025-09625-5 · Cited by 1 · see citing works
Sex differences in morphine sensitivity of neuroligin-3 knockout mice
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- Authors
- Kight, K. E., Argue, K. J., Bumgardner, J. G., Bardhi, K., Waddell, J., & McCarthy, M. M.
- Affiliations
- University of Maryland, Baltimore (US)
- Venue
- Behavioral Neuroscience
- Published
- 2021-12
- Volume
- 135
- Issue
- 6
- Pages
- 782-803
- ISSN
- 0735-7044 (ISSN-L)
- 1939-0084
- PMC
- PMC8649076
- OpenAlex
- W3185587553
- Cited by
- 17
- References
- 121
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 5 · 2023: 4 · 2021: 1
- FWCI
- 1.41
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Behavioral Neuroscience (publishedVersion, other-oa)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Simons Foundation (402378)
- National Institute of Mental Health (R01MH091424)
- National Institute of Child Health and Human Development (P01HD085928)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- neurodevelopmental disorders, autism spectrum disorder, social behavior, social play, ultrasonic vocalizations, nurturing, food retrieval, learning deficits, Pavlovian learning, haploinsufficiency, synaptic proteins, social cognition
- MeSH terms
- Autism Spectrum Disorder, Animals, Female, Learning, Male, Social Behavior, Rats, Sprague-Dawley, Mice, Rats, Neurodevelopmental Disorders
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