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Peering into the Dynamics of Social Interactions: Measuring Play Fighting in Rats
Published on: January 18, 2013
Social Play Behavior Is Critical for the Development of Prefrontal Inhibitory Synapses and Cognitive Flexibility in
Ate Bijlsma1,2, Azar Omrani1,3, Marcia Spoelder2
1Department of Biology, Faculty of Science, Utrecht University, 3584 CH, Utrecht, The Netherlands.
Insights
Social play deprivation in juvenile rats reduces inhibitory synapses in the prefrontal cortex (PFC). This impacts adult cognitive strategies, though partial play can rescue some behaviors.
Area of Science:
- Neuroscience
- Developmental Biology
- Behavioral Science
Background:
- Early life sensory experiences shape neural circuit development.
- Social play is a prominent behavior during postweaning development in rodents.
- The prefrontal cortex (PFC) is crucial for complex cognitive functions.
Purpose of the Study:
- To investigate the impact of social play deprivation on prefrontal cortex (PFC) development.
- To determine if social play is essential for establishing proper PFC connectivity.
- To link PFC synaptic changes to adult cognitive performance.
Main Methods:
- Social play deprivation in male rats from postnatal day 21-42.
- Electrophysiological recordings of synaptic currents in medial PFC layer 5 cells.
- Probabilistic reversal learning (PRL) task to assess cognitive function.
- Histological analysis of inhibitory synapses.
Main Results:
- Social play deprivation (SPD) led to reduced inhibitory synaptic currents in the adult PFC.
- A decrease in perisomatic inhibitory synapses from parvalbumin-positive GABAergic cells was observed in SPD rats.
- SPD rats exhibited a simplified strategy and improved performance in the PRL task.
- Partial daily play during SPD partially rescued PRL performance but not PFC synaptic deficits.
Conclusions:
- Unrestricted juvenile social play is vital for the development of PFC inhibitory synapses.
- Social play deprivation has lasting effects on PFC circuitry and cognitive flexibility.
- The relationship between PFC synaptic structure and complex cognitive behaviors is intricate.
Abstract:
Sensory driven activity during early life is critical for setting up the proper connectivity of the sensory cortices. We ask here whether social play behavior, a particular form of social interaction that is highly abundant during postweaning development, is equally important for setting up connections in the developing prefrontal cortex (PFC). Young male rats were deprived from social play with peers during the period in life when social play behavior normally peaks [postnatal day 21-42] (SPD rats), followed by resocialization until adulthood. We recorded synaptic currents in layer 5 cells in slices from medial PFC of adult SPD and control rats and observed that inhibitory synaptic currents were reduced in SPD slices, while excitatory synaptic currents were unaffected. This was associated with a decrease in perisomatic inhibitory synapses from parvalbumin-positive GABAergic cells. In parallel experiments, adult SPD rats achieved more reversals in a probabilistic reversal learning (PRL) task, which depends on the integrity of the PFC, by using a more simplified cognitive strategy than controls. Interestingly, we observed that one daily hour of play during SPD partially rescued the behavioral performance in the PRL, but did not prevent the decrease in PFC inhibitory synaptic inputs. Our data demonstrate the importance of unrestricted social play for the development of inhibitory synapses in the PFC and cognitive skills in adulthood and show that specific synaptic alterations in the PFC can result in a complex behavioral outcome.SIGNIFICANCE STATEMENT This study addressed the question whether social play behavior in juvenile rats contributes to functional development of the prefrontal cortex (PFC). We found that rats that had been deprived from juvenile social play (social play deprivation - SPD) showed a reduction in inhibitory synapses in the PFC and a simplified strategy to solve a complex behavioral task in adulthood. Providing one daily hour of play during SPD partially rescued the cognitive skills in these rats, but did not prevent the reduction in PFC inhibitory synapses. Our results demonstrate a key role for unrestricted juvenile social play in PFC development and emphasize the complex relation between PFC circuit connectivity and cognitive function.

