Oscillations and hippocampal-prefrontal synchrony

Abstract

The hippocampus, a structure required for many types of memory, connects to the medial prefrontal cortex, an area that helps direct neuronal information streams during intentional behaviors. Increasing evidence suggests that oscillations regulate communication between these two regions. Theta rhythms may facilitate hippocampal inputs to the medial prefrontal cortex during mnemonic tasks and may also integrate series of functionally relevant gamma-mediated cell assemblies in the medial prefrontal cortex. During slow-wave sleep, temporal coordination of hippocampal sharp wave-ripples and medial prefrontal cortex spindles may be an important component of the process by which memories become hippocampus-independent. Studies using rodent models indicate that oscillatory phase-locking is disturbed in schizophrenia, emphasizing the need for more studies of oscillatory synchrony in the hippocampal-prefrontal network.

Figure 1

Hippocampal theta and sharp wave-ripples coordinate neuronal activity in mPFC. (a) mPFC spikes are modulated by CA1 theta phase. An example field potential recording from CA1 is shown in black; the corresponding theta filtered recording is shown superimposed in red. Spikes recorded simultaneously from a mPFC neuron are shown below (vertical blue lines). Modified and reproduced from [25^•], with permission from Nature Publishing Group, Macmillan Publishers Ltd (http://www.nature.com). (b) Schematic illustrating the modulation of mPFC gamma amplitude by hippocampal theta phase [18^••,22,30]. Note that this effect was not measured in the study from which the theta recordings in (a) were obtained [25^•]; thus, hippocampal theta phase values (dashed vertical blue lines) depicted here for illustration of the general effect may not be accurate. (c) Simultaneous mPFC (blue) and CA1 (red) LFP recordings during slow-wave sleep are depicted above corresponding single unit recordings. Note that when sharp wave-ripples are apparent in the CA1 LFP recordings, synchronous bursts of mPFC and CA1 single unit activity can also be seen. Modified and reproduced from [40], with permission from Elsevier (http://www.sciencedirect.com/science/journal/08966273).

Figure 2

Average coherence spectra for simultaneous LFP recordings from mPFC and ventral hippocampus (blue), dorsal and ventral hippocampi (gray), and mPFC and dorsal hippocampus (purple) in wild-type mice running between 7 and 15 cm/s in a familiar arena. Shaded areas indicate 95% confidence intervals, and the red line at the bottom indicates the level of coherence expected by chance (p < 0.05). Note that two peaks can be seen in the gamma range, at ~50 and 100 Hz (indicated by arrows), in the coherence spectrum for simultaneous mPFC–ventral hippocampal recordings. Modified and reproduced from [18^••], with permission from Elsevier (http://www.sciencedirect.com/science/journal/08966273).

Figure 3

Average coherence spectra for simultaneous LFP recordings from mPFC and CA1 in wild-type (gray) and Df(16)A^+/− (green) mice. Shaded areas indicate the standard error of the mean. Coherence during the choice phase of a working memory task is shown on the left, while coherence during habituation sessions is shown on the right. CA1-mPFC coherence was reduced in mutant mice. Note that theta (~5 Hz) and slow sgamma (~45 Hz) coherence tended to be higher in wild-type mice when working memory processes were engaged. Modified and reproduced from [25^•], with permission from Nature Publishing Group, Macmillan Publishers Ltd (http://www.nature.com).