Two star mazes, but a single representation of space in the monkey hippocampus

International audienceHow does the brain code similarities between different experiences while also discriminating their specificity? Studies of spatial memory have provided ample evidence that different episodes are coded by distinct patterns of cell activity. In the rodent foraging for food, hippocampal cells signal the animal's location through a place field. These place fields change when elements of the environment are altered, and a global remapping occurs when the animal is placed in different enclosures. Here we asked how hippocampal cells in the monkey code two virtual reality environments bearing a similarity of structure but different visual landmarks. We previously showed that the primate hippocampus codes space during wayfinding in more complex ways than simple place-coding, and includes task-related information, among which the progression towards the goal (Wirth et al., 2017, PLoS Biol 15(2): e2001045). We now compare the activity maps obtained when the animal searches for a hidden reward in a familiar, well-known star maze vs. a novel maze of same shape, but differing in the visible landmarks. We showed that while 35% coded only one environment, 29% of cells coded both environments. In 71% of the latter cells, activity maps showed a higher cross-correlation than expected by chance between the familiar and the novel maze. Thus, while physical landmarks changed, these cells maintained a goal-centered and task-related representation of space. This abstract representation progressively formed as a function of learning, as the cross-correlation steadily increased across learning epochs. Crucially, this progression was apparent when decoding cell activity in task-related state space or goal-centered physical space, but not as a function of either view direction or point of gaze. To summarize, some cells abstracted from the physical details of the maps and only coded high-level, goal-and task-related information in schema-like representation; the other maze-selective cells could concurrently represent the uniqueness of the perceptual and/or episodic experience

Gaze-informed, task-situated representation of space in primate hippocampus during virtual navigation.

To elucidate how gaze informs the construction of mental space during wayfinding in visual species like primates, we jointly examined navigation behavior, visual exploration, and hippocampal activity as macaque monkeys searched a virtual reality maze for a reward. Cells sensitive to place also responded to one or more variables like head direction, point of gaze, or task context. Many cells fired at the sight (and in anticipation) of a single landmark in a viewpoint- or task-dependent manner, simultaneously encoding the animal's logical situation within a set of actions leading to the goal. Overall, hippocampal activity was best fit by a fine-grained state space comprising current position, view, and action contexts. Our findings indicate that counterparts of rodent place cells in primates embody multidimensional, task-situated knowledge pertaining to the target of gaze, therein supporting self-awareness in the construction of space

Sensitivity to landmark identity and relative distance.

<p><b>Left panel</b>. Activity of a cell for each of the four landmarks viewed at four intervals of relative distances on the entry path (RD1 to RD4, see <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.2001045#sec017" target="_blank">Materials and Methods</a>). Top row: schema of the maze with these distance intervals illustrated as areas for each landmark (southwestern landmark in blue, northwestern in red, northeastern in green, and southeastern in black). The pictures above the rasters show a still image of the monkey’s view of the landmark at each relative distance symbolized by dotted lines on the raster (12, 8, 4), the last one being at 0. Each raster represents the activity of the cell to each landmark as the animal moves forward in the corresponding path. On these rasters, each line is a trial. The bottom graph shows the average cell activity over all trials. <b>Right panel</b>. Activity of a different cell recorded during the same session as the cell shown in <b>the Left panel</b>. Underlying data can be found at <a href="http://dx.doi.org/10.6080/K0R49NQV" target="_blank">http://dx.doi.org/10.6080/K0R49NQV</a>.</p

Individual examples of cell activity in the four coding spaces studied.

<p>Each space is mapped in a column (columns 1–4). The top row describes the structure of each of the coding spaces: monkey self-position (position), virtual head direction (direction), flattened gaze map (point of gaze), and state space (state space). Note that the state-space graph is drawn so that a sector like the one highlighted in green contains all the moves in which the monkey faces in the same direction (here, towards the northeastern landmark). Rows 2 to 9 represent the activity of eight individual cells that illustrate different firing patterns. The far-right column represents a raster histogram of the activity of each cell for all the laps that occurred in the path highlighted in red on the far-left figure for cells 3, 4, 7, and 8 or in black on the right adjacent figure for cells 1, 2, 5, and 6. In this raster representation, each row corresponds to an individual trial, and each tick represents an action potential, on a time window of 2.5 s. Monkey identity is indicated with mS or mK on the position maps. Underlying data can be found at <a href="http://dx.doi.org/10.6080/K0R49NQV" target="_blank">http://dx.doi.org/10.6080/K0R49NQV</a>.</p

State-space selectivity.

<p><b>A.</b> Schematics illustrating the analysis method whereby activities corresponding to the same location (maze center) and direction (dashed sector) were compared on the different state-space transitions (in red). <b>B</b>. Histogram of the state-space selectivity indices across the responsive cells. Cells significantly invariant to current transition are in blue; cells significantly context-dependent are in red (permutation tests). The distribution of indices for the surrogate spike sets is shown in dashed green. <b>C–D</b>. State-space maps (restricted to the center) of two context-dependent cells. Underlying data can be found at <a href="http://dx.doi.org/10.6080/K0R49NQV" target="_blank">http://dx.doi.org/10.6080/K0R49NQV</a>.</p

Landmark viewpoint-invariant versus viewpoint-dependent cells.

<p>Top row: schematics of the monkey’s five different viewpoints for either the landmark immediately left or the landmark immediately right from the reward location. For every path, the landmark appears either on the animal’s left or right. <b>A–C</b>. Individual examples of cell activity (average and trial-by-trial raster histogram; cells numbered as in <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.2001045#pbio.2001045.g002" target="_blank">Fig 2</a>) aligned on the landmark’s left or right entries in the animal’s field of view. The color codes correspond to the activity on the individual paths identified in the top row. Cells displayed in <b>A</b> and <b>C</b> discriminate between different viewpoints, while the cell displayed in <b>B</b> does not. <b>D.</b> Path selectivity index calculated for the different viewpoints of the landmark left or right of the reward (best landmark for each cell). In red are cells for which the index was significantly higher from chance (viewpoint dependent), and in blue are cells for which the index was significantly lower than chance (viewpoint invariant). The distribution of indices for the surrogate spike sets is shown in dashed green. Underlying data can be found at <a href="http://dx.doi.org/10.6080/K0R49NQV" target="_blank">http://dx.doi.org/10.6080/K0R49NQV</a>.</p

Experimental setup and behavioral task.

<p><b>A.</b> Experimental setup. The animal was seated in front of a 152 x 114 cm screen on which a computer-generated scene was projected in stereo. The animal was equipped with shutter glasses synchronized with the projection and could move in the virtual world via a joystick. A juice dispenser delivered reward directly in the animal’s mouth when the monkey reached a hidden rewarded area. <b>B.</b> View from above of the star maze. Five landmarks were placed between the five arms of the maze at a radius twice the arms’ length. A reward was given to the animal when he reached the end of an arbitrarily chosen arm (in this case, the arm between the sunflower and the house). <b>C.</b> A sequential illustration of the animal’s position and field of view at key representative events of a trial. (1) The animal starts at one end of a path and moves towards the center, (2) turns left or right in the center, (3) chooses one path, (4) enters the chosen path and is rewarded at the end if correct, and (5) the animal is relocated (joystick disengaged) to the next start. <b>D.</b> First-person view of the five events described in <b>C</b>, with a heat map of the monkey’s gaze fixations overlaid on the scene illustrating the animal’s scanning interests. Arrows indicate the main direction of motion of the animal. <b>E.</b> Illustration of the steps described in <b>C</b> and <b>D</b> in the actual maze space. Monkey’s moves are represented by colored arrows. <b>F.</b> Illustration of the state space in which neuronal data was analyzed. The same steps as in <b>E</b> are plotted in the state-space graph with corresponding colors. For convenience, the animal’s current position in the graph also denotes the animal’s current straight ahead direction. For example, a position in the northeastern part of the graph corresponds to the animal viewing the northeast from its physical position. The state-space representation parses the animal’s trajectories into a series of action- or position-triggered transitions between choice points (graph vertices). Starting positions are figured as black dots. All actions that can eventually lead to the reward are in solid lines, while dashed lines indicate either erroneous actions leading to the end of unrewarded arms (open circles) or the path to the next start, outside the maze arms. This representation allows describing in a similar way the moves that include a translation and the purely rotational moves made in the center of the maze (expanded inset in the black square). Rotations of 72° (angle between two maze arms) are mapped to the central part of the graph, with counterclockwise rotations innermost (e.g., in red). Rotations of 36° (angle between landmark and maze arm) are mapped to the outer circular arcs (either clockwise or counterclockwise; e.g., in cyan). <b>G.</b> Mapping the animal’s 3-D point of regard. Left: three-dimensional schematic of the maze (green), monkey (brown), and point of gaze (red dot). Blue rectangles represent the location of the landmarks. For ease of representation, we define an invisible cylindrical wall running through the landmark centroids. Right: convention for the flattened representation of the point-of-gaze map. When directed further than the distance to the landmark wall, the point of gaze was computed as directed towards this wall; then, in a second step, this wall was flattened as an annulus to create the final 2-D map. <b>H.</b> Heat map of the point of gaze, overlaid on a schematic of the maze for one session (monkey S). The regions of interest explored by the animal are the ends of the paths, the landmarks, and the rewarded area.</p

Des usages aux pratiques : le Web a-t-il un sens ?

Cet ouvrage, issu des travaux du groupe TIC-IS de la Société Française des Sciences de l’Information et de la Communication, a pour objectif de mettre en évidence de nouvelles approches avec les théories des systèmes, de la non-linéarité et de la complexité, afin d’appréhender plus facilement le développement d’Internet et des réseaux numériques. En effet, l’extraordinaire développement de ces réseaux est marqué par un double mouvement d’expansion et de fragmentation Les relations entre acteurs évaluent, et s’il est aujourd’hui facile et rapide d’accéder à un large ensemble d’informations, le niveau de qualité des données « disponibles » est inégal. L’ambition de ce volume est d’approfondir la réflexion autour de plusieurs perspectives : comment les informations naissent-elles et circulent-elles ? Comment les réseaux évoluent-ils ? Quelles interactions pour favoriser les stratégies économiques, territoriales et/ou professionnelles ? Quelles pratiques et/ou usages pour favoriser l’émergence de projets durables ? Comment mettre en place une construction collective des connaissances ? Les textes réunis témoignent des enjeux de la recherche sur le numérique en sciences de l’information et de la communication : quelles directions ? quelles significations ? Le Web a-t-il un sens