Predictors of successful memory encoding in the human hippocampus and amygdala
In daily life, humans witness a large number of events. We remember some of these past events in great detail whereas others are forgotten within minutes. What determines what we remember and what we forget? Behaviorally, we tend to remember best those events that were high in salience- that is, rewarding, threatening, surprising or novel.
At the level of single neurons, however, it is unclear what sequence of events leads to the storage of a new memory. In particular it is unclear whether mechanisms that induce synaptic plasticity (e.g. LTP/LTD) in vitro and in vivo are utilized at the level of populations of neurons to encode a new memory. Whether a sequence of action potentials induces plasticity depends on when the pre-synaptic neuron fires relative to the activity of its neighbors. In the hippocampus, stimulation leads to LTP only if stimulated at the peak of the theta (4-8 Hz) oscillations. Whether this mechanism is also at work for natural stimuli is unknown.
We recorded extracellular neural activity from the MTL of epileptic patients, who had electrodes implanted for the purpose of localizing seizures. We simultaneously recorded single-unit activity and the local field potential (LFP) from the amygdala and hippocampus. Patients (n=5) viewed a sequence of unique images. In a later recognition memory test, patients indicated whether they had seen the image before or not on a 6-point confidence scale. Patients had good memory (average d'=1.22) and a good sense of confidence.
Here, we focus on neural activity during learning. First, we compared the LFP power between stimuli that were later remembered and stimuli that were forgotten. We found that power differences in several distinct frequency bands were predictive of memory formation: delta (<3 Hz), theta (4-8 Hz), alpha (8-12Hz) as well as gamma (>25 Hz). Also, we trained a decoder on learning trials for which the memory test followed shortly after learning. We then used this decoder to predict whether the patient will remember a separate set of stimuli 24 h later. The decoder performed significantly above chance. Thus, LFP power differences can be used to predict successful memory formation.
We further observed that a substantial fraction of single units fired action potentials that were phase-locked to the theta as well as the gamma band. Can differential phase locking explain why LFP power differences are a good indicator of memory formation? We computed the spike-field coherence (SFC) for each unit and found significant peaks in the SFC for theta as well as gamma frequencies. Comparing the SFC between subsequently remembered and forgotten stimuli shows a larger SFC for later remembered stimuli. This indicates that tight coordination between stimulus-evoked neuronal firing and the activity of the local population is crucial for successful memory formation. Since the SFC is normalized for both the number of spikes as well as local power changes, this further indicates that coordination beyond oscillation power increases is a prerequisite for memory formation.
Conference:
Computational and systems
neuroscience 2009, Salt Lake City, UT, United States, 26 Feb - 3 Mar, 2009.
Presentation Type:
Poster Presentation
Topic:
Poster Presentations
Citation:
(2009). Predictors of successful memory encoding in the human hippocampus and amygdala.
Front. Syst. Neurosci.
Conference Abstract:
Computational and systems
neuroscience 2009.
doi: 10.3389/conf.neuro.06.2009.03.092
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Received:
02 Feb 2009;
Published Online:
02 Feb 2009.