Hippocampal function and brain oscillations
The importance of brain oscillations for hippocampal learning was first suggested by the fact that tetanic stimulus protocols effective in producing LTP in vitro are similar to hip- pocampal theta rhythms in vivo. It is now clear that modulations in gamma frequency (30–100 Hz) and theta frequency (4–8 Hz) bands and in phase relations between them can provide the synchrony needed to generate LTP in the hippocampus and control information flow that brings about encoding or retrieval of information.
Gamma oscillations of hippocampal pyramidal cell membrane potential arise from rhythmic inhibition imposed by activity in local GABAergic hub interneurons. The effectiveness of incoming excitatory inputs to the pyramidal cell is greatest when it occurs out of phase with the inhibition and this synchronizes the cells subjected to the gamma inhibition to fire within 10 ms of each other. This has several effects:
- It can generate STDP (10–20 ms is the necessary time window).
- If the synchronized cells converge onto downstream neurons their near simultaneous activity will result in significant temporal summation increasing the probability in which the downstream neuron will fire.
- Because stronger excitatory inputs overwhelm inhibition more easily than weak ones, more active neurons spike earlier during a gamma band oscillation than weakly activated neurons. While the gamma oscillations sort inputs so in which the stronger arrive downstream earlier than the weak ones.
Theta oscillations can be produced by hippocampal neural networks in isolation but normally it requires cholinergic input from the septum which makes pyramidal cells more excitable.
Correlations between theta and gamma oscillations are important. In rats learning associations among places and items for instance when we consider which place cells are acquiring their place fields the amplitude of gamma oscillations is frequency modulated by the theta oscillations instance example the size of the gamma spikes rises and falls in phase with the theta rhythm. These correlations can be associated to models of how the hippocampus works.
Gamma activity falls into two frequency bands, low and high. Low-frequency gamma in CA1 coincides with the falling phase of the theta band oscillations and is synchronous with low-frequency gamma in CA3. High-frequency gamma in CA1 happens during the rising phase of the theta band and is synchronized with high-frequency gamma in the entorhinal cortex. Therefore theta rhythms seem to play a role in controlling information flow by entorhinal cortex and CA3 to CA1: inputs to CA1 from memory-related recurrent processing in CA3 occurs at one phase of theta and is characterized through low gamma frequency coherence, although sensory-related input from the entorhinal cortex occurs at a different theta phase and is characterized through high gamma coherence. These two different patterns are thought to correspond to different phases of the theta rhythm being required for encoding or retrieval in CA1, with encoding corresponding to input from the entorhinal cortex although retrieval corresponds to CA3 input.
Hippocampal oscillations also influence activity in other fields. In the duration of spatial learning tasks theta activity coherent with that in the hippocampus is seen in the prefrontal cortex and the ventral striatum. In somatosensory and medial prefrontal regions bursts of locally produced gamma oscillations are shortly coherent with hippocampal theta rhythms during exploration and REM sleep. Synchronous activity in the gamma band is seen in the medal temporal lobe of rodents and primates including humans during memory tasks.