Oscillatory correlates of memory in non-human primates

Abstract

The ability to navigate through our environment, explore with our senses, track the passage of time, and integrate these various components to form the experiences which make up our lives is shared among humans and animals. The use of animal models to study memory, coupled with electrophysiological techniques that permit the direct measurement of neural activity as memories are formed and retrieved, has provided a wealth of knowledge about these mechanisms. Here, we discuss current knowledge regarding the specific role of neural oscillations in memory, with particular emphasis on findings derived from non-human primates. Some of these findings provide evidence for the existence in the primate brain of mechanisms previously identified only in rodents and other lower mammals, while other findings suggest parallels between memory-related activity and processes observed in other cognitive modalities, including attention and sensory perception. Taken together, these results provide insight into how network activity may be organized to promote memory formation, and suggest that key aspects of this activity are similar across species, providing important information about the organization of human memory.

Keywords: Gamma; Hippocampus; Medial temporal lobe; Monkeys; Oscillations; Theta.

Fig. 1

Hippocampal gamma-band oscillations related to memory. (a) Visual Preferential Looking Task design from Jutras et al., 2009. Two-hundred unique stimuli were presented in each test session, with up to 8 trials intervening between the first and second presentations. Each trial began with a required 1 second fixation period and trials were separated by a 1 second inter-trial interval. (b) Spike-field coherence as a function of time and frequency for an example neuron-LFP pair, for high recognition (top) and low recognition (bottom) trials. Coherence (52-68 Hz) was significantly enhanced during the encoding of subsequently well-recognized stimuli. (c) Gamma-band spike-field coherence expressed as percentage of baseline averaged over 175 hippocampal recording pairs, during high recognition (red) and low recognition (blue) trials, as a function of time from stimulus onset. Red and blue shaded areas represent SEM. Gray shaded area represents time points at which gamma-band coherence was significantly different for the two conditions (p < 0.01). (d) Temporal-order task design from Naya and Suzuki, 2011. A sequence of two cue stimuli was presented in the encoding phase. The two cue items and one distractor were presented at three different randomly–determined positions in the response phase. Monkeys were rewarded for touching the two cue items in the same temporal order as they were presented in the encoding phase. Dashed circles indicate correct targets. (e) Two-dimensional plot of the population average LFP spectrogram in the hippocampus (n = 62). Red pixels indicate time-frequency domains in which activity was stronger than that in the control period (lasting from 150 to 100 ms before cue 1 onset). Blue pixels indicate the opposite pattern. The differential activities were evaluated by t values (paired t test). Gray bars indicate times of cue presentation.

Fig. 2

Learning and immediate novelty signals of the monkey LFP and human fMRI (from Hargreaves et al., 2012). (a) Bar graphs depicting the results of the monkey entorhinal LFP multiple regression analyses comparing mean β values across different learning strengths (red), reference (blue), and initial presentation (gray) trials for the beta-band (10-25 Hz) spectra. (b) Same as (a), but for the monkey hippocampal LFP multiple regression analyses. (c) Results of the human entorhinal fMRI BOLD signal multiple regression analyses comparing mean β values across the different learning strengths (red), reference (blue), and initial presentation (gray) trials. (d) Same as (c), but for the human hippocampal fMRI BOLD signal multiple regression analyses. **p < 0.01, ***p < 0.0005.

Fig. 3

Theta oscillations in the monkey hippocampus (from Jutras et al., in press). (a) A representative example of one monkey’s scan path from the Visual Preferential Looking Task, showing that the monkey spent more time looking at the image when it was novel (yellow) compared to when it was repeated (blue). Circles represent points of fixation between saccades, with the size of each circle proportional to the duration of the fixation period. (b) Power spectra for two example LFP channels across all VPLT blocks, showing peaks around 8-11 Hz. (c) Examples of theta bouts during VPLT performance. For each example, the theta bout in the raw LFP is marked by a gray square, and the power spectrogram of the LFP signal is presented below. (d) Autocorrelograms of each example LFP shown in (c), during the theta bout. (e) Raw (red) and theta (3-12 Hz) filtered segments (blue) from an example LFP, showing reset to a consistent phase following saccade onset. (f) Phase concentration for the 400-ms period centered on saccade onset for High and Low Recognition conditions, for an example LFP. (g) Power spectrograms from one example LFP, during the 800 ms time period immediately preceding stimulus presentation. (h) Modulation of theta power for High and Low Recognition trials across 114 LFPs. The area of significant power modulation across conditions is outlined in black.