Abstract
Whether from a fall, sports concussion, or even combat injury, there is a critical need to identify when an individual is able to return to play or work following traumatic brain injury (TBI). Electroencephalogram (EEG) and local field potentials (LFP) represent potential tools to monitor circuit-level abnormalities related to learning and memory: specifically, theta oscillations can be readily observed and play a critical role in cognition. Following moderate traumatic brain injury in the rat, lasting changes in theta oscillations coincide with deficits in spatial learning. We hypothesized, therefore, that theta oscillations can be used as an objective biomarker of recovery, with a return of oscillatory activity corresponding with improved spatial learning. In the current study, LFP were recorded from dorsal hippocampus and anterior cingulate in awake, behaving adult Sprague Dawley rats in both a novel environment on post-injury days 3 and 7, and Barnes maze spatial navigation on post-injury days 8–11. Theta oscillations, as measured by power, theta-delta ratio, peak theta frequency, and phase coherence, were significantly altered on day 3, but had largely recovered by day 7 post-injury. Injured rats had a mild behavioral phenotype and were not different from shams on the Barnes maze, as measured by escape latency. Injured rats did use suboptimal search strategies. Combined with our previous findings that demonstrated a correlation between persistent alterations in theta oscillations and spatial learning deficits, these new data suggest that neural oscillations, and particularly theta oscillations, have potential as a biomarker to monitor recovery of brain function following TBI. Specifically, we now demonstrate that oscillations are depressed following injury, but as oscillations recover, so does behavior.
Highlights
At least 3.8 million traumatic brain injuries (TBI) occur each year [1, 2], costing an estimated $221 billion annually, with ∼95% of that cost attributed to long-term care [3]
Theta is a large, slow wave oscillation (5–12 Hz) that can be measured in the non-invasive electroencephalogram (EEG) and recordings of local field potentials (LFP) from depth electrodes implanted in brain regions such as the hippocampus [24,25,26,27]
Even with a significant delay between injury and evaluation, there was a significant effect of group on righting time [F(3, 38) = 8.618, p < 0.001], due to both the traumatic brain injury (TBI) (1068.3 ± 89.4 s, p < 0.05) and 7.7 Hz (1276.6 ± 102.0 s, p < 0.001) groups having significantly longer recovery times compared to sham (681.7 ± 98.0 s, Figure 2B)
Summary
At least 3.8 million traumatic brain injuries (TBI) occur each year [1, 2], costing an estimated $221 billion annually, with ∼95% of that cost attributed to long-term care [3]. Theta is a large, slow wave oscillation (5–12 Hz) that can be measured in the non-invasive electroencephalogram (EEG) and recordings of local field potentials (LFP) from depth electrodes implanted in brain regions such as the hippocampus [24,25,26,27]. Hippocampal theta oscillations synchronize activity both within local networks and across distal cortical regions involved in cognitive processing [28, 29]. In both humans and rats, theta power increases during the acquisition phase of spatial and object-based learning tasks [30,31,32]. Chemical- [41, 42] or injury-induced [43, 44] inhibition of theta oscillations leads to cognitive dysfunction, and cross frequency relationships with gamma (28–64 Hz) waves are implicated in memory encoding and recall [45]
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