Neural Correlates of Object-in-Place Learning in Hippocampus and Prefrontal Cortex

Abstract

Hippocampus and prefrontal cortex (PFC) process spatiotemporally discrete events while maintaining goal-directed task demands. Although some studies have reported that neural activities in the two regions are coordinated, such observations have rarely been reported in an object-place paired-associate (OPPA) task in which animals must learn an object-in-place rule. In this study, we recorded single units and local field potentials simultaneously from the CA1 subfield of the hippocampus and PFC as rats learned that object A, but not object B, was rewarded in place 1, but not in place 2 (vice versa for object B). Both hippocampus and PFC are required for normal performance in this task. PFC neurons fired in association with the regularity of the occurrence of a certain type of event independent of space, whereas neuronal firing in CA1 was spatially localized for representing a discrete place. Importantly, the differential firing patterns were observed in tandem with common learning-related changes in both regions. Specifically, once OPPA learning occurred and rats used an object-in-place strategy, (i) both CA1 and PFC neurons exhibited spatially more similar and temporally more synchronized firing patterns, (ii) spiking activities in both regions were more phase-locked to theta rhythms, (iii) CA1-mPFC coherence in theta oscillation was maximal before entering a critical place for decision making. The results demonstrate differential as well as common neural dynamics between hippocampus and PFC in acquiring the OPPA task and strongly suggest that both regions form a unified functional network for processing an episodic event.

Dissociable effects of NR2A and NR2B NMDA receptor antagonism on cognitive flexibility but not pattern separation

“…As used here, PAL involves the encoding and retrieval of object-location information. Performance in this task may be linked to hippocampal and prefrontal cortical function as shown in rats (Kim et al 2011;Talpos et al 2014) and humans studies (de Rover et al 2011;Hales et al 2009;Owen et al 1995) using a similar paired associate learning task. Surprisingly, NVP-AAM077 did not show improvement or impairment on this task, especially as MK-801 produced robust impairments in PAL.…”

Medial prefrontal-perirhinal cortical communication is necessary for flexible response selection

“…Consistent with this hypothesis is the observation that disconnection lesions of the PFC and inferotemporal cortex in monkeys impair delayed nonmatching-to-sample performance (Browning, Baxter, and Gaffan, 2013) and object-in-place scene memory (Wilson, Gaffan, Mitchell, and Baxter, 2007). Additional evidence for a unified mPFC-PER network that supports performance on the OPPA task is that the theta rhythm in the mPFC and hippocampus becomes more synchronized after acquisition of the OPPA task rule (Kim, Delcasso, and Lee, 2011). Because there are limited direct projections from mPFC to dorsal hippocampus, this synchrony may require that information flows through the rhinal cortices, thus making the PER an integral part of this circuit.…”

The evolution of episodic memory

“…A study by Wood et al (108) showed that different subsets of neurons selectively coded for "what" (e.g., a specific odor) and "where" (e.g., a specific location) information whereas others coded for specific what-where conjunctions (a specific odor in a particular place). More recent studies have shown that the emergence of what-where coding parallels the learning of item-place associations (109,110). Although lesions studies suggest what-where integration depends on subregion CA3 but not CA1 (34), what-where neural coding has been reported in both subregions with no significant differences reported (108,109).…”