Tracking the Course of Hippocampal Representations during Learning: When Is the Map Required?

Abstract

Distinct ensembles of hippocampal cells can be active in numerous contexts, but specific ‘cognitive maps’ tend to be retrieved on repeat visits to the same place. During aging, the reliability of map retrieval in CA1 networks is reduced; this provides a unique opportunity to investigate correlations between inconsistent activity patterns in circuits hypothesized to enable context encoding and hippocampus-dependent learning ability. Here, CA1 pyramidal cells were recorded in six young and six old rats while memory for specific locations was probed using a place-dependent eyeblink conditioning task. Rats were conditioned twice daily for 31 days, during which a total of 8259 and 7042 cells were recorded from young and old rats, respectively. Spontaneous remapping, a change in location of the majority of place fields between two consecutive sessions in the same environment, was observed in two young rats and four old rats during this task, but only after at least 13 days of training. Under these conditions the altered network representation did not result in loss of spatial accuracy of the blink, and in fact those rats with the best place conditioning remapped the most, whereas those with the best memory in a spatial water maze task remapped the least. These results suggest that when the hippocampal representation for a particular context is weak or unstable, such as can occur in senescence, extra-hippocampal systems that mediate alternate learning strategies are more likely to dominate behavior.

The Aging Navigational System

“…These connections functionally couple coactive cells at the time of encoding so that later activation of a sufficient subset will propagate to all members of the cell assembly resulting in a complete reinstantiation of the learned pattern. As mentioned above, old rats show distinct differences in the stability of their cognitive maps as assessed by ensemble recordings of CA1 hippocampal neurons (Barnes et al, 1997; Schimanski et al, 2013). Aged rats occasionally generate a new and distinct place cell representations for a familiar environment (Barnes et al, 1997; Schimanski et al, 2013) – that is, they occasionally retrieve ‘the wrong map’ (Figure 2A; Figure 3).…”

“…As mentioned above, old rats show distinct differences in the stability of their cognitive maps as assessed by ensemble recordings of CA1 hippocampal neurons (Barnes et al, 1997; Schimanski et al, 2013). Aged rats occasionally generate a new and distinct place cell representations for a familiar environment (Barnes et al, 1997; Schimanski et al, 2013) – that is, they occasionally retrieve ‘the wrong map’ (Figure 2A; Figure 3). The inability to represent an identical environment as the same place may indicate excessive pattern separation in the aged CA1 region.…”

“…In fact, even though there is mixed evidence regarding an association between age-related changes in hippocampal volume and memory function (van Petten, 2004), several studies have reported changes in place cell firing characteristics. For example, old rats show differences in the stability of their cognitive maps as assessed by ensemble recordings of hippocampal neurons (Barnes et al, 1997; Schimanski et al, 2013). CA1 hippocampal pyramidal cells in aged rats occasionally generate a new and distinct place cell representation for a familiar environment (Barnes et al, 1997; Schimanski et al, 2013), and these cells take significantly longer to begin to show consistent spatial firing, even in familiar environments (Hok et al, 2012).…”

“…Place-field maps of young animals are highly correlated between consecutive exposures while aged animals occasionally showed uncorrelated firing, indicative of remapping. When the proportion of rats that remapped between morning and afternoon sessions was tracked over 31 days (Schimanski et al, 2013), maps were stable between sessions until day 14, when both age groups began to show periodic remapping episodes, with aged animals remapping more frequently. Aged rats also show reduced spatial navigation accuracy in the Morris Water Maze task (Lindner, 1997) (bottom right, shows performance for rats from age 1.3 to 26.3 months old).…”

Distinguishing adaptive plasticity from vulnerability in the aging hippocampus

“…In awake, behaving animals, however, CA1 single unit firing rates are similar in young and aged rats (Schimanski et al, 2013). Again, this observation suggests that changes may occur to combat the effects of increased CA3 drive in order to preserve normal network activity.…”