Anterior/Posterior Competitive Deactivation/Activation Dichotomy in the Human Hippocampus as Revealed by a 3D Navigation Task

Abstract

Anterior/posterior long axis specialization is thought to underlie the organization of the hippocampus. However it remains unclear whether antagonistic mechanisms differentially modulate processing of spatial information within the hippocampus. We used fMRI and a virtual reality 3D paradigm to study encoding and retrieval of spatial memory during active visuospatial navigation, requiring positional encoding and retrieval of object landmarks during the path. Both encoding and retrieval elicited BOLD activation of the posterior most portion of hippocampus, while concurrent deactivations (recently shown to reflect decreases in neural responses) were found in the most anterior regions. Encoding elicited stronger activity in the posterior right than the left hippocampus. The former structure also showed significantly stronger activity for allocentric vs. egocentric processing during retrieval. The anterior vs. posterior pattern mimics, from a functional point, although at much distinct temporal scales, the previous anatomical findings in London taxi drivers, whereby posterior enlargement was found at the cost of an anterior decrease, and the mirror symmetric findings observed in blind people, in whom the right anterior hippocampus was found to be larger, at the cost of a smaller posterior hippocampus, as compared with sighted people. In sum, we found a functional dichotomy whereby the anterior/posterior hippocampus shows antagonistic processing patterns for spatial encoding and retrieval of 3D spatial information. To our knowledge, this is the first study reporting such a dynamical pattern in a functional study, which suggests that differential modulation of neural responses within the human hippocampus reflects distinct roles in spatial memory processing.

Slow-theta power decreases during item-place encoding predict spatial accuracy of subsequent context recall

“…Acknowledging the importance of this system for the successful performance of our study's task, by extension, it is plausible that slow theta negative SMEs manifested in actively engaged brain regions. In agreement, negative SMEs were significant in posterior hippocampi, which typically show increased BOLD activation during the encoding and retrieval of spatial memories, in contrast with anterior hippocampi (Duarte et al, 2014;Nadel et al, 2013). As an fMRI study applying multivoxel pattern similarity analysis has demonstrated, right posterior hippocampus specifically carries information about spatial locations during the encoding of object location relationships in working memo ry (Libby et al, 2014).…”

Neurofunctional topography of the human hippocampus

“…Most have theorized that the right hippocampus is primarily engaged in spatial processing (i.e., 3D spatial navigation, or remembering an object location), while the left is more attuned to verbal information (Duarte et al, 2014; Greve et al, 2011). Additionally, lateralization appears to be preserved (i.e., dissociable roles of the hippocampus have been hypothesized in spatial navigation across species (Copara et al, 2014; Ekstrom et al, 2003; Gagliardo et al, 2005; Hami et al, 2014; Herold et al, 2014; Klur et al, 2009)), and has been linked to gender differences in humans (Persson et al, 2013).…”

“…This proposed segmentation has been given new life in recent years, with investigations into cell organization and gene expression (Fanselow and Dong, 2010; Poppenk et al, 2013), all supporting a potential differentiation along an anterior to posterior gradient. Corroborating evidence has also emerged from the fields of magnetic resonance spectroscopy (MRS) (King et al, 2008) and functional magnetic resonance imaging (fMRI) (Duarte et al, 2014; Duncan et al, 2014; Greve et al, 2011; Prince et al, 2005; Strange et al, 2005). For example, Prince and colleagues (Prince et al, 2005) demonstrated strong evidence for an anterior-posterior parcellation that corresponded to an encoding-retrieval gradient.…”

“…It was not until the early 1990's that H.M. received a magnetic resonance imaging scan that revealed potential discrepancies in the neurosurgical account of his lesions, which were confirmed following his death when more sophisticated imaging procedures could be carried out (Annese et al, 2014; Augustinack et al, 2014). Additionally, most, if not all, studies of hippocampal subspecialization limit their investigations to a single behavioral domain (e.g., cognition) or a single paradigm that compares specific neurocognitive processes (i.e., encoding versus retrieval) (Duarte et al, 2014; Duncan et al, 2014; Prince et al, 2005). Thus, we have relied on inferences about hippocampal topography drawn from data in non-human species, from case studies, and/or from focused cognitive processing (i.e., memory or spatial navigation) studies.…”

Sex Hormones and Cognition: Neuroendocrine Influences on Memory and Learning

“…Notably, the dorsal hippocampus of rodents is equivalent to the posterior hippocampus of primates (591). For example, the posterior region of the human hippocampus is activated during retrieval of an allocentric cognitive map (135,142,285). In this regard, it is intriguing that London taxi cab drivers, who undergo years of extensive spatial training to learn the intricate streets of London, England show growth in the posterior, but not anterior, hippocampus (398).…”