The anterior versus posterior hippocampal oscillations debate in human spatial navigation: evidence from an electrocorticographic case study

Abstract

IntroductionHippocampal oscillations have been regularly described as playing a dominant role in spatial memory and navigation in rodents. In humans, the relative role of anterior versus posterior rhythms during navigational memory is not established.MethodsHere, we tested this hypothesis using direct brain ECoG recordings in the anterior and posterior hippocampus of a patient, in a navigational task requiring spatial memory. We assessed multiple oscillatory bands during encoding and retrieval phases.ResultsWe found navigation related 1–3.5 Hz activity during retrieval, both in the anterior and posterior hippocampus. Activity between 4 and 8 Hz was identified during both encoding and retrieval, only in the anterior hippocampus.ConclusionsOur findings are consistent with the view that an anterior/posterior functional gradient is present in the hippocampus, and involves two distinct neuronal networks, supporting either encoding or retrieval processes. Although this is a single case scenario, these findings suggest that neural oscillations during spatial navigation do vary across hippocampal subregions, as a function of encoding versus retrieval processes during the mnemonic process. In this single case study, the results point to the presence of a dual involvement of multiple frequency bands across hippocampal subregions during encoding and retrieval. Although these results need generalization, they provide a new perspective on distinct physiological properties of the anterior and posterior hippocampus in human spatial navigation during encoding and retrieval.

Intracranial recordings in humans reveal specific hippocampal spectral and dorsal vs. ventral connectivity signatures during visual, attention and memory tasks

“…Previous reports found a crucial role of hippocampal slow EEG frequencies during sleep in the memory consolidation processes 24 . In the same line, our previous work and others demonstrated a link between theta oscillations and self-motion information and spatial-memory 25 , 26 and an association between high-frequency patterning and recognition memory 17 , 23 . In spite of the identified links between activity across different frequency bands and distinct brain functions 27 , 28 , little is known in relation to their relevance to network organization, as defined by functional connectivity approaches.…”

“…We recorded these intracranial data while patients were task engaged (example video available as supplementary material 1 , (patient wearing a cap and positioned to prevent identification). This real-time scenario in long recording periods provides a unique opportunity to evaluate the brain in a naturalistic manner, unlike other less ecological and more rigid experimental approaches 26 .…”

“…We have used an approach that takes advantage of the invasive large scale recordings while patients perform distinct visual and/or memory related tasks for long periods of time. We were able to visualize patterns of activation and functional connectivity of the human hippocampus during real-life recordings and this provides a new framework to understand the role of the hippocampus in cognition 11 , 26 .…”

Delayed injury of hippocampal interneurons after neonatal hypoxia‐ischemia and therapeutic hypothermia in a murine model

“…However, the protection of the male PV+ INs within the CA1 region by TH eight days after HI was not homogenous throughout the whole hippocampus, with greater protection in the posterior hippocampus than in the anterior hippocampus. Long-axis specialization studies suggest a functional dichotomy between the anterior and posterior hippocampus (Duarte et al, 2016; Duarte et al, 2014; Lepore et al, 2009; Maguire et al, 2000). While anterior hippocampus is involved in encoding and spatial learning; the posterior hippocampus is involved in memory retrieval and spatial navigation.…”

Cortical functional topography of high-frequency gamma activity relates to perceptual decision: an Intracranial study

“…Invasive recordings are often used in the clinical context [ 30 , 35 ]. They provide a unique opportunity to measure brain signals at high temporal and spatial resolution [ 34 , 36 – 38 ]. This technique has been widely used to study high frequency activity [ 34 , 39 , 40 ] that cannot be uncovered by scalp EEG and their putative functional correlates have been widely debated [ 9 , 10 , 20 , 24 , 37 ].…”