Hippocampal θ dysfunction after lateral fluid percussion injury

Abstract

Chronic memory deficits are a major cause of morbidity following traumatic brain injury (TBI). In the rat, the hippocampal theta rhythm is a well-studied correlate of memory function. This study sought to investigate disturbances in hippocampal theta rhythm following lateral fluid percussion injury in the rat. A total of 13 control rats and 12 TBI rats were used. Electrodes were implanted in bilateral hippocampi and an electroencephalogram (EEG) was recorded while the rats explored a new environment, and also while navigating a modified version of the Barnes maze. Theta power and peak theta frequency were significantly attenuated in the injured animals. Further, injured rats were less likely to develop a spatial strategy for Barnes maze navigation compared to control rats. In conclusion, rats sustaining lateral fluid percussion injury demonstrated deficits in hippocampal theta activity. These deficits may contribute to the underlying memory problems seen in chronic TBI.

FIG. 1.

Positions of electrodes on the rat's skull. The large open circle shows the craniectomy defect for the lateral fluid percussion injury. The small dark circles show where the recording electrodes where implanted. The stars represent the dural reference leads. The plus signs illustrate where small screws where placed to fix the electrodes and acrylic to the skull.

FIG. 2.

The modified Barnes maze. The animals were placed under the start box in the middle of the table. The peripheral circles represent holes in the table. The black circle represents the location of the escape compartment.

FIG. 3.

Electrode placement. A diagram of coronal sections of the rat hippocampus where the distal recoding electrodes were found on histology. They are arranged rostral to caudal (1–9). This illustrates all of the electrodes included in the analysis for all rats.

FIG. 4.

Spectral power waveforms. The average spectral power waveforms for control and lateral fluid percussion injured rats in (A) the New Environment condition, and (B) the Dark Environment condition. (C) A sample raw electroencephalographic recording of theta rhythm (TBI, traumatic brain injury).

FIG. 5.

Theta power in the New Environment condition. The left panel summarizes total theta power summed from 6–10 Hz for control and TBI rats for all electrodes. The center panel summarizes theta power by hemisphere: ipsilateral (Ipsi) and contralateral (Contra). The right panel summarizes theta power by electrode depth: superficial (Sup) and deep (*p < 0.05 compared to control animals; TBI, traumatic brain injury).

FIG. 6.

Theta power in the Dark Environment condition. The left panel summarizes total theta power summed from 6–10 Hz for control and TBI rats for all electrodes. The center panel summarizes theta power by hemisphere: ipsilateral (Ipsi) and contralateral (Contra). The right panel summarizes theta power by electrode depth: superficial (Sup) and deep (TBI, traumatic brain injury).

FIG. 7.

Barnes maze performance. Data points are the average escape latencies for injured and control rats over subsequent Barnes maze trials (TBI, traumatic brain injury).

FIG. 8.

Barnes maze search strategies. Shown are the numbers of control (A) or TBI (B) animals for each Barnes maze trial using random, peripheral, and spatial search strategies. Chi-square analysis collapsing data across all trials revealed a significant difference in the distribution of search patterns between the TBI and control groups (p < 0.001; TBI, traumatic brain injury).