3 research outputs found
Place cells dynamically refine grid cell activities to reduce error accumulation during path integration in a continuous attractor model
Navigation is one of the most fundamental skills of animals. During spatial navigation, grid cells in the medial entorhinal cortex process speed and direction of the animal to map the environment. Hippocampal place cells, in turn, encode place using sensory signals and reduce the accumulated error of grid cells for path integration. Although both cell types are part of the path integration system, the dynamic relationship between place and grid cells and the error reduction mechanism is yet to be understood. We implemented a realistic model of grid cells based on a continuous attractor model. The grid cell model was coupled to a place cell model to address their dynamic relationship during a simulated animal’s exploration of a square arena. The grid cell model processed the animal’s velocity and place field information from place cells. Place cells incorporated salient visual features and proximity information with input from grid cells to define their place fields. Grid cells had similar spatial phases but a diversity of spacings and orientations. To determine the role of place cells in error reduction for path integration, the animal’s position estimates were decoded from grid cell activities with and without the place field input. We found that the accumulated error was reduced as place fields emerged during the exploration. Place fields closer to the animal’s current location contributed more to the error reduction than remote place fields. Place cells’ fields encoding space could function as spatial anchoring signals for precise path integration by grid cells.Fil: Fernandez Leon, Jose Alberto. Universidad Nacional del Centro de la Provincia de Buenos Aires. Centro de Investigaciones en FĂsica e IngenierĂa del Centro de la Provincia de Buenos Aires. - Consejo Nacional de Investigaciones CientĂficas y TĂ©cnicas. Centro CientĂfico TecnolĂłgico Conicet - Tandil. Centro de Investigaciones en FĂsica e IngenierĂa del Centro de la Provincia de Buenos Aires. - Provincia de Buenos Aires. GobernaciĂłn. ComisiĂłn de Investigaciones CientĂficas. Centro de Investigaciones en FĂsica e IngenierĂa del Centro de la Provincia de Buenos Aires; ArgentinaFil: Uysal, Ahmet Kerim. Baylor College of Medicine; Estados UnidosFil: Ji, Daoyun. Baylor College of Medicine; Estados Unido
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Grid cell co-activity patterns remain stable across different behavioral states and experiences
Grid cells in the medial entorhinal cortex have been well studied while animals are exploring their environment; however, what they do when an animal is not navigating is less clear. Other cell types in the entorhinal-hippocampal network appear to have memory-related activity when an animal is inactive, so what grid cells do during quiescence is an important question. If grid cells show activity similar to place cells during rest and sleep, then it would imply that grid cells play an active role in memory functions rather than simply providing current sensory information to the hippocampus. Models have been proposed that make testable predictions about grid cell activity when spatial input is absent. The continuous attractor network model of grid cell pattern formation posits that grid cell patterning is a result of network connections between grid cells. As a result of this connectivity, these models hypothesize that grid cell co-activity patterns should be the same during sleep as during active navigation. In my first study, I investigated how spike time correlations between grid cell pairs during sleep compared to spike time correlations between the same grid cell pairs during waking activity. I found
that the same correlation patterns were present regardless of whether spatial information was available to grid cells (i.e., during active navigation) or whether sensory input was absent (i.e., during sleep). These results support the continuous
attractor network model hypothesis. In my second study, I examined whether novel experience changed grid cell co-activity patterns during active waking behaviors, rest, and sleep. I found that spike time correlations between grid cell pairs remained stable across behavioral states regardless of experience. In my last study, I looked at organized sequences of firing in grid cell ensembles to
examine whether small changes in correlations led to detectable changes in more complex ensemble representations of experience. I found that grid cell ensemble activity did not appear to be influenced by different behaviors or novel experience. Taken together, these results suggest that grid cells are part of a low-dimensional, continuous attractor network and that grid cell activity patterns during sleep reflect connections in the grid cell network rather than representing specific experiences.Neuroscienc
The Neural Basis of a Cognitive Map
It has been proposed that as animals explore their environment they build and maintain a cognitive map, an internal representation of their surroundings (Tolman, 1948). We tested this hypothesis using a task designed to assess the ability of rats to make a spatial inference (take a novel shortcut)(Roberts et al., 2007). Our findings suggest that rats are unable to make a spontaneous spatial inference. Furthermore, they bear similarities to experiments which have been similarly unable to replicate or support Tolman’s (1948) findings. An inability to take novel shortcuts suggests that rats do not possess a cognitive map (Bennett, 1996). However, we found evidence of alternative learning strategies, such as latent learning (Tolman & Honzik, 1930b) , which suggest that rats may still be building such a representation, although it does not appear they are able to utilise this information to make complex spatial computations.
Neurons found in the hippocampus show remarkable spatial modulation of their firing rate and have been suggested as a possible neural substrate for a cognitive map (O'Keefe & Nadel, 1978). However, the firing of these place cells often appears to be modulated by features of an animal’s behaviour (Ainge, Tamosiunaite, et al., 2007; Wood, Dudchenko, Robitsek, & Eichenbaum, 2000). For instance, previous experiments have demonstrated that the firing rate of place fields in the start box of some mazes are predictive of the animal’s final destination (Ainge, Tamosiunaite, et al., 2007; Ferbinteanu & Shapiro, 2003). We sought to understand whether this prospective firing is in fact related to the goal the rat is planning to navigate to or the route the rat is planning to take. Our results provide strong evidence for the latter, suggesting that rats may not be aware of the location of specific goals and may not be aware of their environment in the form of a contiguous map. However, we also found behavioural evidence that rats are aware of specific goal locations, suggesting that place cells in the hippocampus may not be responsible for this representation and that it may reside elsewhere (Hok, Chah, Save, & Poucet, 2013).
Unlike their typical activity in an open field, place cells often have multiple place fields in geometrically similar areas of a multicompartment environment (Derdikman et al., 2009; Spiers et al., 2013). For example, Spiers et al. (2013) found that in an environment composed of four parallel compartments, place cells often fired similarly in multiple compartments, despite the active movement of the rat between them. We were able to replicate this phenomenon, furthermore, we were also able to show that if the compartments are arranged in a radial configuration this repetitive firing does not occur as frequently. We suggest that this place field repetition is driven by inputs from Boundary Vector Cells (BVCs) in neighbouring brain regions which are in turn greatly modulated by inputs from the head direction system. This is supported by a novel BVC model of place cell firing which predicts our observed results accurately.
If place cells form the neural basis of a cognitive map one would predict spatial learning to be difficult in an environment where repetitive firing is observed frequently (Spiers et al., 2013). We tested this hypothesis by training animals on an odour discrimination task in the maze environments described above. We found that rats trained in the parallel version of the task were significantly impaired when compared to the radial version. These results support the hypothesis that place cells form the neural basis of a cognitive map; in environments where it is difficult to discriminate compartments based on the firing of place cells, rats find it similarly difficult to discriminate these compartments as shown by their behaviour.
The experiments reported here are discussed in terms of a cognitive map, the likelihood that such a construct exists and the possibility that place cells form the neural basis of such a representation. Although the results of our experiments could be interpreted as evidence that animals do not possess a cognitive map, ultimately they suggest that animals do have a cognitive map and that place cells form a more than adequate substrate for this representation