Dynamic coding of dorsal hippocampal neurons between tasks that differ in structure and memory demand

Abstract

Hippocampal place fields show remapping between environments that contain sufficiently different contextual features, a phenomenon that may reflect a mechanism for episodic memory formation. Previous studies have shown that place fields remap to changes in the configuration of visual landmarks in an environment. Other experiments have demonstrated that remapping can occur with experience, even when the visual features of an environment remain stable. A special case of remapping may be trajectory coding, the tendency for hippocampal neurons to exhibit different firing rates depending upon recently visited or upcoming spatial locations. To further delineate the conditions under which different task features elicit remapping, we recorded from place cells in dorsal CA1 of hippocampus while rats switched between tasks that differed in memory demand and task structure; continuous spatial alternation (CA), delayed spatial alternation (DA), and tactile-visual conditional discrimination (CD). Individual hippocampal neurons and populations of simultaneously recorded neurons showed coherent remapping between CA and CD. However, task remapping was rarely seen between DA and CD. Analysis of individual units revealed that even though the population retained a coherent representation of task structure across the DA and CD tasks, the majority of individual neurons consistently remapped at some point during recording sessions. In contrast with previous studies, trajectory coding on the stem of the T-maze was virtually absent during all of the tasks, suggesting that experience with multiple tasks in the same environment reduces the likelihood that hippocampal neurons will represent distinct trajectories. Trajectory coding was, however, observed during the delay period of DA. Whether place fields change in response to task or trial type or remain stable within the same environment may depend on which aspects of the context are most salient or relevant to behavior.

Hippocampal Signatures of Episodic Memory: Evidence from Single-Unit Recording Studies

“…The most robust demonstrations of trajectory coding have been seen in continuous spatial alternation (Wood et al, 2000; Lee et al, 2006) and serial reversal tasks (Ferbinteanu and Shapiro, 2003). Interestingly, some tasks that are known to depend on the hippocampus, such as delayed spatial alternation do not elicit robust trajectory coding (Ainge et al, 2007a; Griffin et al, 2012; Hallock and Griffin, 2013). This set of findings argues against the interpretation of trajectory coding being a memory signal used in task performance.…”

“…Ainge et al (2012) compared prospective coding across behaviorally identical tasks and showed no differences in the coding behavior of hippocampal neurons between the memory-guided and cue-guided conditions. Conversely, a recent study showed that a large percentage of hippocampal neurons remapped between continuous alternation and conditional discrimination tasks, a phenomenon that was termed “task remapping” (See Figure 1; Hallock and Griffin, 2013). When a delay was added to the alternation task, however, there was very little remapping between tasks, suggesting that the temporal structure of the task (discrete vs. continuous trials) was driving the place cell remapping rather than the memory demand of the task (Hallock and Griffin, 2013).…”

“…The population showed the same task remapping pattern as the neuron in (A) : high correlation values between sets of continuous alternation trials and low correlation values across the conditional discrimination and continuous alternation tasks. Data adapted from Hallock and Griffin (2013). …”

“…Upon introduction to a circular track, hippocampal neurons show little directionally dependent variation in firing rate; as rats gain more experience on the track, trajectory coding develops over time (Navratilova et al, 2012). Finally, when rats are trained on both continuous alternation and conditional discrimination in a T-maze, trajectory coding on the maze stem is virtually absent when the rat switches between the two tasks, indicating that experience during task training has a large influence on whether or not trajectory coding will be observed (Hallock and Griffin, 2013). In this same study, prospective trajectory coding was seen when rats switched between delayed alternation and conditional discrimination tasks on the same T-maze.…”

Still searching for the engram

“…Place cell maps were observed in both strategies but the cells participating and their firing patterns in the same maze were unrelated (Eschencko & Mizumori, 2007); similar remapping has been observed in animals switching between response and object choice strategies (Lee & Kim 2010) and between objects or positions of the same objects within an environment (Muzzio et al, 2009). Remapping has also been observed in a T-maze delayed non-matching to place task where distinct firing patterns were observed between sample trials, where the animal must encode its path, and choice trials, where the animal must remember the correct path (Griffin et al, 2007; also see Hallock and Griffin, 2013). In yet another task, remapping was observed when rats switched between start and goal arms while performing the same spatial memory task in the same maze (Bahar et al, 2011).…”