SummaryWe determined how learning modifies neural representations in primary visual cortex (V1) during acquisition of a visually guided behavioral task. We imaged the activity of the same layer 2/3 neuronal populations as mice learned to discriminate two visual patterns while running through a virtual corridor, where one pattern was rewarded. Improvements in behavioral performance were closely associated with increasingly distinguishable population-level representations of task-relevant stimuli, as a result of stabilization of existing and recruitment of new neurons selective for these stimuli. These effects correlated with the appearance of multiple task-dependent signals during learning: those that increased neuronal selectivity across the population when expert animals engaged in the task, and those reflecting anticipation or behavioral choices specifically in neuronal subsets preferring the rewarded stimulus. Therefore, learning engages diverse mechanisms that modify sensory and non-sensory representations in V1 to adjust its processing to task requirements and the behavioral relevance of visual stimuli.

Grid cells represent an animal's location by firing in multiple fields arranged in a striking hexagonal array 1 . Such a profound and constant regularity prompted suggestions that grid cells represent a universal and environment-invariant metric for navigation 1,2 . Originally the properties of grid-patterns were believed to be independent of the shape of the environment and this notion has dominated all mainstream theoretical grid cell models [3][4][5][6] . Nonetheless several studies indicate that environmental boundaries influence grid-firing 7-10 though the strength, nature and longevity of this effect is unclear. Here, we show that grid orientation, scale, symmetry and homogeneity are strongly and permanently affected by environmental geometry. We found that grid-patterns orient to the walls of polarised enclosures such as squares but not circles. Furthermore, the hexagonal grid symmetry is permanently broken in highly polarised environments such as trapezoids, the pattern being more elliptical and less homogeneous. Our results provide compelling evidence for the idea that environmental boundaries compete with the internal organisation of the grid cell system to drive grid firing. Importantly, grid cell activity is more local than previously thought and as a consequence cannot provide a universal spatial metric in all environments.

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...

Climbing fiber input produces complex spike synchrony across populations of cerebellar Purkinje cells oriented in the parasagittal axis. Elucidating the fine spatial structure of this synchrony is crucial for understanding its role in the encoding and processing of sensory information within the olivocerebellar cortical circuit. We investigated these issues using in vivo multineuron two-photon calcium imaging in combination with information theoretic analysis. Spontaneous dendritic calcium transients linked to climbing fiber input were observed in multiple neighboring Purkinje cells. Spontaneous synchrony of calcium transients between individual Purkinje cells falls off over ϳ200 m mediolaterally, consistent with the presence of cerebellar microzones organized by climbing fiber input. Synchrony was increased after administration of harmaline, consistent with an olivary origin. Periodic sensory stimulation also resulted in a transient increase of synchrony after stimulus onset. To examine how synchrony affects the neural population code provided by the spatial pattern of complex spikes, we analyzed its information content. We found that spatial patterns of calcium events from small ensembles of cells provided substantially more stimulus information (59% more for seven-cell ensembles) than available by counting events across the pool without taking into account spatial origin. Information theoretic analysis indicated that, rather than contributing significantly to sensory coding via stimulus dependence, correlational effects on sensory coding are dominated by redundancy attributable to the prevalent spontaneous synchrony. The olivocerebellar circuit thus uses a labeled line code to report sensory signals, leaving open a role for synchrony in flexible selection of signals for output to deep cerebellar nuclei.

Grid cells are neurons active in multiple fields arranged in a hexagonal lattice and are thought to represent the "universal metric for space." However, they become nonhomogeneously distorted in polarized enclosures, which challenges this view. We found that local changes to the configuration of the enclosure induce individual grid fields to shift in a manner inversely related to their distance from the reconfigured boundary. The grid remained primarily anchored to the unchanged stable walls and showed a nonuniform rescaling. Shifts in simultaneously recorded colocalized grid fields were strongly correlated, which suggests that the readout of the animal's position might still be intact. Similar field shifts were also observed in place and boundary cells-albeit of greater magnitude and more pronounced closer to the reconfigured boundary-which suggests that there is no simple one-to-one relationship between these three different cell types.