Hippocampal gamma oscillations increase with memory load

Abstract

Although the hippocampus plays a crucial role in encoding and retrieval of contextually mediated episodic memories, considerable controversy surrounds the role of the hippocampus in short-term or working memory. To examine both hippocampal and neocortical contributions to working memory function, we recorded electrocorticographic activity from widespread cortical and subcortical sites as 20 neurosurgical patients performed working memory tasks. These recordings revealed significant increases in 48-90 Hz gamma oscillatory power with memory load for two classes of stimuli: letters and faces. Sites exhibiting gamma increases with memory load appeared primarily in the hippocampus and medial temporal lobe. These findings implicate gamma oscillatory activity in the maintenance of both letters and faces in working memory and provide the first direct evidence for modulation of hippocampal gamma oscillations as humans perform a working memory task.

Figure 1.

Schematic of the Sternberg task. Participants see a list of 1–4 stimuli (faces or letters), followed by a 3000 ms delay interval. After the delay, a probe stimulus appears and participants have to indicate whether the probe was a member of the just-presented list. The maintenance interval is defined as the period between 0 and 3000 ms after the offset of the last list item. Stimuli were sets of 16 letters and 16 faces, presented in alternating blocks of 15 lists.

Figure 2.

Single electrode analyses by region of interest during the maintenance interval. Fraction of electrodes showing a significant increase (solid) or decrease (dotted) of oscillatory power with memory load. The gray line indicates the fraction of significant electrodes in the permuted data. The frequency bands are as follows: delta (δ), 2–4 Hz; theta (θ), 4–9 Hz; alpha (α), 9–14 Hz; beta (β), 14–28 Hz; low gamma (γ₁), 28–48 Hz; mid-gamma (γ₂), 48–90 Hz; high gamma (γ₃), 90–100 Hz.

Figure 3.

Cortical electrodes showing significant increases (red) and decreases (blue) in 48–90 Hz gamma power with memory load. Circles, Faces; crosses, letters. Electrodes not showing a significant load effect in this frequency band are drawn in black. Hippocampal electrodes are not shown.