Saccades during visual exploration align hippocampal 3–8 Hz rhythms in human and non-human primates

Kari L Hoffman,Timothy K Leonard,Rodrigo Montefusco-Siegmund,Michelle C Dragan,Taufik A Valiante,Cristiano Micheli

doi:10.3389/fnsys.2013.00043

Abstract

Visual exploration in primates depends on saccadic eye movements (SEMs) that cause alternations of neural suppression and enhancement. This modulation extends beyond retinotopic areas, and is thought to facilitate perception; yet saccades may also influence brain regions critical for forming memories of these exploratory episodes. The hippocampus, for example, shows oscillatory activity that is generally associated with encoding of information. Whether or how hippocampal oscillations are influenced by eye movements is unknown. We recorded the neural activity in the human and macaque hippocampus during visual scene search. Across species, SEMs were associated with a time-limited alignment of a low-frequency (3–8 Hz) rhythm. The phase alignment depended on the task and not only on eye movements per se, and the frequency band was not a direct consequence of saccade rate. Hippocampal theta-frequency oscillations are produced by other mammals during repetitive exploratory behaviors, including whisking, sniffing, echolocation, and locomotion. The present results may reflect a similar yet distinct primate homologue supporting active perception during exploration.

Highlights

For most primates, exploration of the environment is primarily visual, and makes use of the specialized mechanism of saccadic eye movements (SEMs): the rapid and repetitive displacement of a high-acuity region of the retina to sample different locations in the visual environment
Eye movements made in the dark or following simple visual stimuli elicited spiking and/or local field potential (LFP) modulation in subdomains such as the superior temporal polysensory area, the parahippocampal gyrus, inferotemporal cortex, and hippocampus, though the consequences for perception are unclear (Ringo et al, 1994; Sobotka et al, 1997, 2002; Purpura et al, 2003; Bartlett et al, 2011; Jutras et al, 2013)
Eye movements that are concomitant with the onset of new visual information, as occurs during naturalistic visual search, lead to temporal lobe neuronal activity which is phase-locked in the theta-alpha range (Bartlett et al, 2011)

Summary

Introduction

Exploration of the environment is primarily visual, and makes use of the specialized mechanism of saccadic eye movements (SEMs): the rapid and repetitive displacement of a high-acuity region of the retina to sample different locations in the visual environment. Eye movements that are concomitant with the onset of new visual information, as occurs during naturalistic visual search, lead to temporal lobe neuronal activity which is phase-locked in the theta-alpha range (Bartlett et al, 2011) This coupling effect is stronger than that predicted exclusively by the visually-evoked response when decoupled from fixation, and is generally consistent with reports of phase-locking and phasedependent codes in early visual areas (Montemurro et al, 2008; Rajkai et al, 2008; Bosman et al, 2009; Ito et al, 2011). Precise phase-alignment of spiking activity to oscillations in the rodent hippocampus is posited to be relevant for memory encoding, as well (Tort et al, 2009; Shirvalkar et al, 2010; Lisman and Jensen, 2013)

Methods

Results

Conclusion