Hippocampal gamma‐band Synchrony and pupillary responses index memory during visual search

Abstract

Memory for scenes is supported by the hippocampus, among other interconnected structures, but the neural mechanisms related to this process are not well understood. To assess the role of the hippocampus in memory-guided scene search, we recorded local field potentials and multiunit activity from the hippocampus of macaques as they performed goal-directed search tasks using natural scenes. We additionally measured pupil size during scene presentation, which in humans is modulated by recognition memory. We found that both pupil dilation and search efficiency accompanied scene repetition, thereby indicating memory for scenes. Neural correlates included a brief increase in hippocampal multiunit activity and a sustained synchronization of unit activity to gamma band oscillations (50-70 Hz). The repetition effects on hippocampal gamma synchronization occurred when pupils were most dilated, suggesting an interaction between aroused, attentive processing and hippocampal correlates of recognition memory. These results suggest that the hippocampus may support memory-guided visual search through enhanced local gamma synchrony. © 2016 Wiley Periodicals, Inc.

Hippocampal and neocortical oscillations are tuned to behavioral state in freely-behaving macaques

“…In this study, however, we show that theta oscillations in non-human primates ( i ) were not sustained during waking periods, ( ii ) did not track the durations of waking behaviors, and ( iii ) predicted sleep instead of active states. Beta and gamma frequencies, on the other hand, were better predictors for active and walking behaviors, consistent with a role for hippocampal beta/gamma in learning and navigation 11–14,27 . Many of the spiking and high-frequency events commonly associated with theta oscillations such as phase coding 26 , phase precession 20,28 , and gamma-frequency shifts 29 may nevertheless be conserved.…”

Differential generation of saccade, fixation and image onset event-related potentials in the human mesial temporal lobe

“…Although there are limited studies to address this, a human single unit study by Andrillon et al (2016) comparing single unit image onset responses to saccade related responses demonstrated a 100% increase in firing rate after image onset, peaking at 300ms, while saccade related responses demonstrated an earlier increase in spiking, and a more modest firing rate increase of 25-30% following a saccade (Andrillon et al, 2015). Additionally, in the NHP hippocampus, an increase in firing rate is seen following image onset in the same task as the one used here, along with an evoked response and lowfrequency phase clustering (Andrillon et al, 2015;Leonard et al, 2015;Montefusco-Siegmund et al, 2017), similar to the response reported in the current study. Although the human single unit data do suggests a modest increase in firing rate following a saccade, an excess of spike synchrony induced by a modulating input may underlie an increase in apparent firing rate (Ito et al, 2011) following saccades in humans (Andrillon et al, 2015) by biasing spike timing (Anastassiou et al, 2011;Cobb et al, 1995), and not increasing firing rate per se.…”

“…We used a previously reported behavioural paradigm (a change-blindness task) on a new set of participants that incorporates image onset and saccadic search, and has been shown to be MTL dependent (Chau et al, 2011) with neuronal correlates to search and memory localized to the hippocampus (Leonard et al, 2015Montefusco-Siegmund et al, 2017). In this task, scenes were presented with the goal of finding the changing object in the scene.…”

“…the current analysis included all stimuli, without separating old and new items, and hits and misses, all of which have been shown the influence the amplitude of the image-onset response (Fell et al, 2004(Fell et al, , 2008Fernández et al, 1999;Montefusco-Siegmund et al, 2017;Mormann et al, 2005;Paller and McCarthy, 2002). To further characterize the difference in these responses, the phase clustering following stimulus onset was investigated.…”

Volitional Control of Individual Neurons in the Human Brain

“…This increase in SFC was independent of power or firing rate changes, was specific to the direct neurons, and occurred only in learning sessions. In the medial temporal lobe, oscillations in this frequency band are rarely observed and in particular have not been reported in human MTL regions where delta, theta, and gamma frequency activity has been associated with a myriad of behaviors (32,(43)(44)(45) including neuroprosthetic skill learning (20,21). In rodents Lansink and colleagues demonstrated beta oscillations in the hippocampus driven by reward predictive cues, and enhanced by learning (34).…”