Gamma frequency connectivity in frontostriatal networks associated with social preference is reduced with traumatic brain injury

Among the myriad of complications associated with traumatic brain injury (TBI), impairments in social behaviors and cognition have emerged as a significant area of concern. Animal models of social behavior are necessary to explore the underlying brain mechanisms contributing to chronic social impairments following brain injury. Here, we utilize large-scale brain recordings of local field potentials to identify neural signatures linked with social preference deficits following frontal brain injury. We used a controlled cortical impact model of TBI to create a severe bilateral injury centered on the prefrontal cortex. Behavior (social preference and locomotion) and brain activity (power and coherence) during a three-chamber social preference task were compared between sham and injured animals. Sham rats preferred to spend time with a social conspecific over an inanimate object. An analysis of local field oscillations showed that social preference was associated with a significant increase in coherence in gamma frequency band across widespread brain regions in these animals. Animals with a frontal TBI showed a significant reduction in this social preference, visiting an inanimate object more frequently and for more time. Reflecting these changes in social behavior, these animals also showed a significant reduction in gamma frequency (25–60 Hz) coherence associated with social preference.

Our results indicate that disturbance in the gamma band network is associated with reduced social preference following frontal TBI. Importantly, the deficits we observed are network-wide, extending far beyond the focal site of injury. Our study identifies a potential neural signature of social preference that could be manipulated to improve social behaviors and may have translational relevance.