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An altered cognitive strategy associated with reduction of synaptic inhibition in the prefrontal cortex after social play deprivation in rats

Azar Omrani, Ate Bijlsma, Marcia Spoelder, Jeroen P.H. Verharen, Lisa Bauer, Cosette Cornelis, René van Dorland, Louk J.M.J. Vanderschuren, Corette J. Wierenga
doi: https://doi.org/10.1101/2020.05.01.070540
Azar Omrani
1Department of Biology, Faculty of Science, Utrecht University, Utrecht, the Netherlands
3Department of Translational Neuroscience, University Medical Center Utrecht, Utrecht, the Netherlands
4Department of CNS Diseases Research, Boehringer Ingelheim Pharma GmbH & Co KG, Biberach, Germany
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Ate Bijlsma
1Department of Biology, Faculty of Science, Utrecht University, Utrecht, the Netherlands
2Department of Animals in Science and Society, Division of Behavioural Neuroscience, Faculty of Veterinary Medicine, Utrecht University, Utrecht, the Netherlands
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Marcia Spoelder
2Department of Animals in Science and Society, Division of Behavioural Neuroscience, Faculty of Veterinary Medicine, Utrecht University, Utrecht, the Netherlands
5Department of Cognitive Neuroscience, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen Medical Centre, Nijmegen, the Netherlands
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Jeroen P.H. Verharen
2Department of Animals in Science and Society, Division of Behavioural Neuroscience, Faculty of Veterinary Medicine, Utrecht University, Utrecht, the Netherlands
3Department of Translational Neuroscience, University Medical Center Utrecht, Utrecht, the Netherlands
6Helen Wills Neuroscience Institute, Department of Molecular and Cell Biology, University of California Berkeley, Berkeley, CA, USA
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Lisa Bauer
1Department of Biology, Faculty of Science, Utrecht University, Utrecht, the Netherlands
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Cosette Cornelis
2Department of Animals in Science and Society, Division of Behavioural Neuroscience, Faculty of Veterinary Medicine, Utrecht University, Utrecht, the Netherlands
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René van Dorland
1Department of Biology, Faculty of Science, Utrecht University, Utrecht, the Netherlands
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Louk J.M.J. Vanderschuren
2Department of Animals in Science and Society, Division of Behavioural Neuroscience, Faculty of Veterinary Medicine, Utrecht University, Utrecht, the Netherlands
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  • For correspondence: c.j.wierenga@uu.nl l.j.m.j.vanderschuren@uu.nl
Corette J. Wierenga
1Department of Biology, Faculty of Science, Utrecht University, Utrecht, the Netherlands
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  • For correspondence: c.j.wierenga@uu.nl l.j.m.j.vanderschuren@uu.nl
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Abstract

Experience-dependent organization of neuronal connectivity is a critical component of brain development, but how experience shapes prefrontal cortex (PFC) development is unknown. Here, we assessed how social play behaviour, which is highly abundant during post-weaning development, shapes PFC function and connectivity. We subjected juvenile rats to social play deprivation (SPD), followed by resocialization until adulthood. In a PFC-dependent probabilistic reversal learning task, SPD rats earned a similar number of rewards, but achieved more reversals than control rats. Computational trial-by-trial analysis showed that SPD rats displayed a simplified cognitive strategy. In addition, inhibitory synaptic currents were significantly reduced in layer 5 PFC cells of SPD rats, with specific changes in parvalbumin- and cannabinoid receptor 1-positive perisomatic inhibitory synapses. Thus, SPD has a long-lasting impact on PFC inhibition via synapse-specific alterations, associated with simplified cognitive strategies. We conclude that proper PFC development depends on pertinent social experience during a restricted time period.

Competing Interest Statement

The authors have declared no competing interest.

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Posted May 03, 2020.
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An altered cognitive strategy associated with reduction of synaptic inhibition in the prefrontal cortex after social play deprivation in rats
Azar Omrani, Ate Bijlsma, Marcia Spoelder, Jeroen P.H. Verharen, Lisa Bauer, Cosette Cornelis, René van Dorland, Louk J.M.J. Vanderschuren, Corette J. Wierenga
bioRxiv 2020.05.01.070540; doi: https://doi.org/10.1101/2020.05.01.070540
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An altered cognitive strategy associated with reduction of synaptic inhibition in the prefrontal cortex after social play deprivation in rats
Azar Omrani, Ate Bijlsma, Marcia Spoelder, Jeroen P.H. Verharen, Lisa Bauer, Cosette Cornelis, René van Dorland, Louk J.M.J. Vanderschuren, Corette J. Wierenga
bioRxiv 2020.05.01.070540; doi: https://doi.org/10.1101/2020.05.01.070540

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