Neural Representations of Location Composed of Spatially Periodic Bands

Abstract

The mammalian hippocampal formation (HF) provides neuronal representations of environmental location, but the underlying mechanisms are unclear. We report a class of cells with spatially periodic firing patterns composed of plane waves (or bands) drawn from a discrete set of orientations and wavelengths. The majority of cells recorded in parasubicular and medial entorhinal cortices of freely moving rats belonged to this class. Grids cells form an important subset, corresponding to hexagonal configurations of bands, and having the most stable firing. Occasional changes between hexagonal and non-hexagonal firing patterns imply a common mechanism underlying the various spatial patterns. Our results indicate a Fourier-like spatial analysis underlying neuronal representations of location, and suggest that path integration is performed by integrating displacement along a restricted set of directions.Place cells in the hippocampus represent the animal's location by firing in discrete environmental locations(1), whereas grid cells are active in multiple locations that form a hexagonally symmetric array covering the entire environment(2), and are found in one of the main inputs to the hippocampus(3, 4), the medial entorhinal cortex (mEC)(2, 5), and also in pre-and parasubiculum (PaS)(5). The spatially periodic firing of grids cells may provide the spatial metric for the hippocampal cognitive map(6, 7), with place cell firing thought to reflect a summation of grid cell inputs(8-11). However, it is unclear how the hexagonal symmetry is generated, whether it represents an entirely unique pattern or one end of a continuum, and whether it is required for spatial representation or reflects other properties such as stability(12) or coding efficiency(13). To examine the spatial periodicity of cells in the parahippocampal region, we recorded 351 cells from superficial layers (II and III) of the medial part of dorsocaudal mEC (5 implants) and adjacent PaS (2 implants) in 7 adult male rats while they foraged for food in a square enclosure (1.3m 2 ; fig. S1). From visual inspection, many of these showed the regular hexagonal pattern characteristic of grid cells (26% passed the standard "gridness" measure(2); Fig. 1A), but a surprisingly large portion * To whom correspondence should be addressed: j.okeefe@ucl.ac.uk. fig. S12). Of these, 37% were grid cells, usually described by three significant Fourier components oriented at multiples of 60° to each other and having similar wavelengths ( Fig. 1F-G, figs. S4-S6). The remaining spatially periodic cells were described by a superposition of one to four significant Fourier components with a greater range of orientations and wavelengths ( Fig. 1G upper in red, figs. S5-S7). Many cells with one or two significant Fourier components (e.g. Fig. 1C, fig. S7) were reminiscent of the band cells postulated as inputs to grid cells in some computational models(12, 15), see also Refs(11,16,17). Europe PMC Funders GroupWe further examined the properties of the spatially periodic non-grid ce...

Grid cells and cortical representation

“…Also, the location of the proposed ring attractors remains elusive. Some grid cells in the deeper MEC layers show somewhat different degrees of periodic firing along the three grid axes 9,26 , raising the possibility that such cells respond to cells with band-like activity 26 , but 'band cells' have not been observed in or near MEC to date.…”

“…1b). Grid cells exhibit variable degrees of asymmetry 24,25 and periodicity may be expressed more strongly along one axis of the triangular grid than the two others 26 . Collectively the variety of grid cells define a map of the animal's relative position in the environment 7,12 .…”

“…The prime challenge is the almost complete lack of excitatory connections between layer II stellate cells, the cell type containing the largest number of grid cells and the most regular grid patterns 9,26,[103][104][105] . Paired recordings have shown that excitatory connections are nearly absent among stellate cells in adult animals and that stellate cells are instead strongly connected via fast-spiking inhibitory interneurons [106][107][108] .…”

Context-dependent spatially periodic activity in the human entorhinal cortex

“…Accordingly, grids recorded in circular or symmetrical enclosures tend to exhibit a narrow range of 60 ± 5°r otational symmetry quantified from autocorrelograms (ACs) (18). However, a comprehensive analysis of spatial periodicity evident from cells in the presubiculum and medial EC of rats revealed that only about 35-50% of medial EC cells exhibited canonical 60°ro-tational symmetry (12% and 28% in the presubiculum and parasubiculum, respectively) (11,22), whereas a significant fraction of medial EC neurons (43%) displayed spatially periodic activity different from the 60°rotational symmetry (11). Nonhexagonal grid structures were most prevalent in enclosures with polarized geometry (20).…”

“…Among the neurons with the greatest spatial specificity are the place cells of the hippocampus (2), head direction cells of the preand postsubiculum (8), border cells in the subiculum and EC (9), and grid cells in the medial EC (10). Although a place cell is only activated when the animal traverses through a unique location in its environment (2), grid-cell activity is elicited in multiple locations that the animal visits (11), and these locations span the environment periodically as vertices of a hexagonal grid formation (10). The two neuroanatomical subsystems are thought to complement each other such that individual place cells represent specific spatial locations and grid cells provide an environment-invariant metric upon which to reference the agent's (animal or human) location (12).…”