Identification of early hippocampal dynamics during recognition memory with independent component analysis.

The hippocampus is generally considered to have relatively late involvement in recognition memory, its main electrophysiological signature being between 400 and 800 ms after stimulus onset. However, most electrophysiological studies have analyzed the hippocampus as a single responsive area, selecting only a single-site signal exhibiting the strongest effect in terms of amplitude. These classical approaches may not capture all the dynamics of this structure, hindering the contribution of other hippocampal sources that are not located in the vicinity of the selected site. We combined intracerebral electroencephalogram recordings from epileptic patients with independent component analysis (ICA) during a recognition memory task involving the recognition of old and new images. We identified two sources with different responses emerging from the hippocampus: a fast one (maximal amplitude at ∼250 ms) that could not be directly identified from raw recordings, and a later one, peaking at ∼400 ms. The earliest component presented different amplitudes between old and new items in 6 out of 10 patients. The latter component had different delays for each condition, with a faster activation (∼290 ms after stimulus onset) for recognized items. We hypothesize that both sources represent two steps of hippocampal recognition memory, the faster reflecting the input from other structures and the latter the hippocampal internal processing. Recognized images evoking early activations would facilitate neural computation in the hippocampus, accelerating memory retrieval of complementary information. Overall, our results suggest that hippocampal activity is composed by several sources with an early activation related to recognition memory. Significance Statement In the human memory circuit, the hippocampus is considered as a structure with relatively late activation, associated to the retrieval of elaborate memories. However, in most electrophysiological studies, it is characterized by the activity of a single contact, which may not represent the entire dynamics of this structure. Here, we combined intracerebral recordings with independent component analysis to separate the activity from two different neural sources generated in the hippocampus. We analyzed the responses of both sources during the recognition of old and new images. Our results reveal new dynamics associated to different neuronal sources within the hippocampus, with recognition memory occurring much faster than previously reported.