Flexible use of allocentric and egocentric spatial memories activates differential neural networks in mice

Abstract

Goal-directed navigation can be based on world-centered (allocentric) or body-centered (egocentric) representations of the environment, mediated by a wide network of interconnected brain regions, including hippocampus, striatum and prefrontal cortex. The relative contribution of these regions to navigation from novel or familiar routes, that demand a different degree of flexibility in the use of the stored spatial representations, has not been completely explored. To address this issue, we trained mice to find a reward relying on allocentric or egocentric information, in a modified version of the cross-maze task. Then we used Zif268 expression to map brain activation when well-trained mice were required to find the goal from a novel or familiar location. Successful navigation was correlated with the activation of CA1, posterior-dorsomedial striatum, nucleus accumbens core and infralimbic cortex when allocentric-trained mice needed to use a novel route. Allocentric navigation from a familiar route activated dorsomedial striatum, nucleus accumbens, prelimbic and infralimbic cortex. None of the structures analyzed was significantly activated in egocentric-trained mice, irrespective of the starting position. These data suggest that a flexible use of stored allocentric information, that allows goal finding even from a location never explored during training, induces a shift from fronto-striatal to hippocampal circuits. Goal-directed navigation is one of the most common and conserved cognitive functions, since the ability to go from one place to another in a complex environment is essential for the survival of most animals. Mammals, including humans, can find their way using multiple different navigational strategies, thought to depend on different brain circuits. Traditionally, the hippocampus has been identified as the region mediating world-centered (allocentric) spatial navigation based on the relative position of landmarks in the environment, while the dorsal striatum has been considered the key structure in body-centered (egocentric) navigation, thought to rely on stimulus-response or procedural processing 1-4. Indeed, lesions of the hippocampus predominantly impair the execution of tasks that require the use of allocentric information, conversely, lesions of the striatum affect tasks dependent on egocentric navigation that requires the association of a particular body turn with the reward 5-9. This view has dominated the field for a long time, but it has been increasingly challenged by accumulating conflicting evidence. It is now well established that a double dissociation exists also within the dorsal striatum, with the dorsolateral (DLS) and the dorsomedial (DMS) compartments mediating respectively procedural versus spatial forms of navigation 10. Spatial cells have been identified in the DMS 11-13 and lesions or pharmacological manipulations of the DMS have been shown to have effects resembling hippocampal lesions 14-17. However, the relative contribution of hippocampus and DMS to allocentric navigation is st...

Unfolding of spatial representation at systems level in infant rats

“…Indeed, the increases in c-Fos activity in hippocampal regions in our Prox group in combination with the positive correlation between CA1 c-Fos levels and locomotor activity in this group, is in line with the assumption that proximal cues alone might be sufficient to regulate hippocampus-based navigation at this age (Rinaldi et al, 2020).…”

Efficacy of Distributed Training Depends on the Dorso-Lateral Striatum

“…In contrast, the dorsolateral striatum (DLS), is critical at later stages of acquisition when performance reaches its asymptotic form 3,4 . Although the striatal complex has been traditionally less investigated in the context of spatial memory 5–7 a similar serial engagement of the two striatal subregions has also been reported with increasing spatial training in the Morris water maze, in both humans and rodents 7 . Thus, a convergence of empirical evidence supports the view that, regardless of the kind of information to be acquired, striatal compartment-specific activity might predict formation of more enduring memories acquired through extensive training.…”

Dissociative Effects of Neuropeptide S Receptor Deficiency and Nasal Neuropeptide S Administration on T-Maze Discrimination and Reversal Learning

“…An explanation for this observation could be that NPS treatment increases excitability of the hippocampus, the brain region involved in allocentric learning [ 62 ]. This may support choosing an allocentric strategy, as well as reversal learning [ 63 ]. In an additional experiment, we confirmed previous findings that nasal NPS administration does not affect locomotor activity ( Figure 3 ).…”