Object and place information processing by CA1 hippocampal neurons of C57BL/6J mice

Abstract

Medial and lateral entorhinal cortices convey spatial/contextual and item/object information to the hippocampus, respectively. Whether the distinct inputs are integrated as one cognitive map by hippocampal neurons to represent location and the objects therein, or whether they remain as parallel outputs, to be integrated in a downstream region, remains unclear. Principal, or complex spike bursting, neurons of hippocampus exhibit location-specific firing, and it is likely that the activity of “place cells” supports spatial memory/navigation in rodents. Consistent with cognitive map theory, the activity of CA1 hippocampal neurons is also critical for nonspatial memory, such as object recognition. However, the degree to which CA1 neuronal activity represents the associations of object-context or object-in-place memory is not well understood. Here, the contributions of mouse CA1 neuronal activity to object recognition memory and the emergence of object-place conjunctive representations were tested using in vivo recordings and functional inactivation. Independent of arena configuration, CA1 place fields were stable throughout testing and object-place representations were not identified in CA1, although the number of fields per cell increased during object sessions, and few object-related firing CA1 neurons (nonplace) were recorded. The results of the inactivation studies confirmed the significant contribution of CA1 neuronal activity to object recognition memory when a delay of 20 min, but not 5 min, was imposed between encoding and retrieval. Together, our results confirm the delay-dependent contribution of the CA1 region to object memory and suggest that object information is processed in parallel with the ongoing spatial mapping function that is a hallmark of hippocampal memory. NEW & NOTEWORTHY We developed variations of the object recognition task to examine the contribution of mouse CA1 neuronal activity to object memory and the degree to which object-context conjunctive representations are formed during object training. Our results indicate that, within the CA1 region, object information is processed in a parallel but delay-dependent manner, with ongoing spatial mapping.

Differential effect of sleep deprivation on place cell representations, sleep architecture, and memory in young and old mice

“…“Context” cells displayed high stability throughout habituation and training; “object configuration” cells remapped when objects were first introduced but remained stable during all the object training sessions; and “unstable” cells remapped across all training sessions. As previously reported, we observed that object configuration cells were active in the context, even before the objects were introduced ( Ásgeirsdóttir et al, 2020 ). Therefore, it is likely that these cells coded the arrangement of the objects in relation to contextual cues already present in the environment, rather than purely object-related firing.…”

Object Recognition Memory: Distinct Yet Complementary Roles of the Mouse CA1 and Perirhinal Cortex

“…Temporary inactivation is an alternative technique that avoids some of the pitfalls of the lesion approach. Previous reports indicate that with a strong object memory protocol, pre-sample, or pre-test, intra-CA1 muscimol impairs object discrimination during the test session (De Lima et al, 2006;Cohen et al, 2013;Stackman et al, 2016;Ásgeirsdóttir et al, 2020). The results of the present regional inactivation studies extend the evidence demonstrating a significant role for CA1 in strong object memory.…”

Flexible encoding of objects and space in single cells of the dentate gyrus

“…78 How these types of object-related activity are processed and utilized within each hippocampal subfield is unclear. The DG may produce conjunctive representations, but the extent to which they are preserved in CA1 is also unclear 3,72,75 and may rely on task demands, similar to the recent finding that activity decorrelation in CA1, but not DG, reflects behavioral discrimination. 79 The DG may participate in a functional pattern separation circuit that is closely associated with distal CA1, 80 which receives preferential LEC inputs and displays more object-related activity.…”

“…[72][73][74] Some of the same types of object-related activity we report here have been observed in other hippocampal regions, such as the LV responses reported in CA1 and CA3. [2][3][4]6,[75][76][77] In contrast to activity changes associated with a single object, LV responses could reflect a mechanism to link the overall geometric relationships between multiple objects and environment boundaries. 78 How these types of object-related activity are processed and utilized within each hippocampal subfield is unclear.…”