Cellular networks underlying human spatial navigation

Abstract

Place cells of the rodent hippocampus constitute one of the most striking examples of a correlation between neuronal activity and complex behaviour in mammals. These cells increase their firing rates when the animal traverses specific regions of its surroundings, providing a context-dependent map of the environment. Neuroimaging studies implicate the hippocampus and the parahippocampal region in human navigation. However, these regions also respond selectively to visual stimuli. It thus remains unclear whether rodent place coding has a homologue in humans or whether human navigation is driven by a different, visually based neural mechanism. We directly recorded from 317 neurons in the human medial temporal and frontal lobes while subjects explored and navigated a virtual town. Here we present evidence for a neural code of human spatial navigation based on cells that respond at specific spatial locations and cells that respond to views of landmarks. The former are present primarily in the hippocampus, and the latter in the parahippocampal region. Cells throughout the frontal and temporal lobes responded to the subjects' navigational goals and to conjunctions of place, goal and view.

Geometric determinants of human spatial memory

“…The experimental paradigm used in the current study provides a new point of contact between neurophysiological studies of spatial representations (Ekstrom et al, 2003;Jeffery et al, 1997;Morris et al, 1982;, animal behavioral studies (Cheng, 1986(Cheng, ,1989Collett et al, 1986;Spetch et al, 1996Spetch et al, , 1997 and psychological investigations (Hermer & Spelke, 1994;King et al, 2002;Shelton & McNamara, 2001;Wang & Spelke, 2000), all of which can be brought to bear in interpreting our findings. Such contact is useful since it means that insights gained at the physiological level can inform experiments at the behavioral level, and vice versa.…”

“…Comparable allocentric representations of physical location (Matsumura et al, 1999) and location of gaze (Rolls, Robertson, & Georges-Francois, 1997) have been reported in non-human primates. The recent discovery of place cells in the human hippocampus (Ekstrom et al, 2003) suggests that some of their properties (discussed below) may be applicable to understanding human spatial behavior. In this virtual navigation task, the firing of many of these cells was modulated according to the current goal.…”

Evidencing a place for the hippocampus within the core scene processing network

“…PHG also shows a greater response to scenes with low, compared with high, feature overlap [Mundy et al, 2012]. Electrophysiological studies in humans also indicate that cells in this region show greater response when viewing spatial landmarks, whereas HC neurons respond to specific locations within an environment [Ekstrom et al, 2003]. Thus, posterior PHG may support navigation via its role in the visual processing of scenes/landmarks [see also Janzen and van Turennout, 2004], rather than coding allocentric position within space [Ekstrom, 2015; Hartley et al, 2003].…”

“…While studies in rodents highlight the HC as critical for spatial navigation and allocentric spatial processing, as evidenced by the presence of place‐selective cells in HC [O'Keefe and Nadel, 1978] and spatial memory deficits following HC lesions [Morris, 1984], the notion that the human HC is involved in scene processing remains controversial [Suzuki, 2009]. While the human HC may be important for navigation [Ekstrom et al, 2003; Maguire et al, 2000; Suthana et al, 2009], its recruitment across a range of mnemonic and perceptual scene processing tasks is indicative of a broader role in scene cognition. Here, too, we localised HC using a working memory task, thus complementing previous studies that find evidence for HC recruitment across a range of cognitive tasks.…”

Le codage de l’espace

“…Les substrats neuronaux de la représentation spatiale découverts chez les rongeurs et présents dans de nombreuses espèces comme le singe ou la chauve-souris existent-t-il également chez l'homme ? Quelques données encore éparses suggèrent l'existence de cellules de lieu et de grille chez l'humain [27][28][29]. La convergence des tests comportementaux entre humains et animaux, par exemple via l'utilisation de la réa-lité virtuelle, laisse envisager le développement d'outils permettant d'évaluer des fonctions cognitives similaires dans différentes espèces.…”