TY - JOUR T1 - Traumatic Brain Injury Preserves Firing Rates but Disrupts Laminar Oscillatory Coupling and Neuronal Entrainment in Hippocampal CA1 JF - eneuro JO - eNeuro DO - 10.1523/ENEURO.0495-19.2020 SP - ENEURO.0495-19.2020 AU - Paul F. Koch AU - Carlo Cottone AU - Christopher D. Adam AU - Alexandra V. Ulyanova AU - Robin J. Russo AU - Maura T. Weber AU - John D. Arena AU - Victoria E. Johnson AU - John A. Wolf Y1 - 2020/07/31 UR - http://www.eneuro.org/content/early/2020/07/31/ENEURO.0495-19.2020.abstract N2 - While hippocampal dependent learning and memory are particularly vulnerable to traumatic brain injury (TBI), the functional status of individual hippocampal neurons and their interactions with oscillations are unknown following injury. Using the most common rodent TBI model and laminar recordings in CA1, we found a significant reduction in oscillatory input into the radiatum layer of CA1 after TBI. Surprisingly, CA1 neurons maintained normal firing rates despite attenuated input, but did not maintain appropriate synchronization with this oscillatory input or with local high frequency oscillations. Normal synchronization between these coordinating oscillations was also impaired. Simultaneous recordings of medial septal neurons known to participate in theta oscillations revealed increased GABAergic/glutamatergic firing rates post-injury under anesthesia, potentially due to a loss of modulating feedback from the hippocampus. These results suggest that TBI leads to a profound disruption of connectivity and oscillatory interactions, potentially disrupting the timing of CA1 neuronal ensembles that underlie aspects of learning and memory.Significance Statement The hippocampus and its connections have been hypothesized to be particularly vulnerable to traumatic brain injury (TBI) and therefore implicated in post-TBI memory impairments. However, it remains an open question whether loss of neurons, their activity, or an encoding disruption underlies such deficits, and whether the remaining neurons are capable of recovering the function of these networks. Using laminar silicon probes spanning the entire CA1 sub-region, this study provides the first in vivo evidence that hippocampal CA1 single unit activity post-TBI can maintain a normal firing rate despite significantly attenuated, layer-specific loss of input. They cannot, however, maintain normal synchronization to the dominant oscillations within the hippocampus, a critical component of hippocampal memory encoding and decoding mechanisms. ER -