The shift from a response strategy to object-in-place strategy during learning is accompanied by a matching shift in neural firing correlates in the hippocampus

Abstract

Hippocampal-dependent tasks often involve specific associations among stimuli (including egocentric information), and such tasks are therefore prone to interference from irrelevant task strategies before a correct strategy is found. Using an object-place paired-associate task, we investigated changes in neural firing patterns in the hippocampus in association with a shift in strategy during learning. We used an object-place paired-associate task in which a pair of objects was presented in two different arms of a radial maze. Each object was associated with reward only in one of the arms, thus requiring the rats to consider both object identity and its location in the maze. Hippocampal neurons recorded in CA1 displayed a dynamic transition in their firing patterns during the acquisition of the task across days, and this corresponded to a shift in strategy manifested in behavioral data. Specifically, before the rats learned the task, they chose an object that maintained a particular egocentric relationship with their body (response strategy) irrespective of the object identity. However, as the animal acquired the task, it chose an object according to both its identity and the associated location in the maze (object-in-place strategy). We report that CA1 neurons in the hippocampus changed their prospective firing correlates according to the dominant strategy (i.e., response versus object-in-place strategy) employed at a given stage of learning. The results suggest that neural firing pattern in the hippocampus is heavily influenced by the task demand hypothesized by the animal and the firing pattern changes flexibly as the perceived task demand changes.[Supplemental material is available online at http://www.learnmem.org.]An event often involves objects placed in particular locations. To form a cognitive representation of such an event, an animal needs to represent many heterogeneous pieces of information such as individual objects, their spatial locations, and also egocentric body movements associated with the navigation through the objects and locations. All the information then needs to be associated in a correct way (e.g., proper object-place association) for successful representation of the event. Processing only a subset of information successfully may lead to an error in identifying the correct event. It is believed that the hippocampus is essential for forming and retrieving such conjunctive representations among stimuli for processing events (O'Reilly and McClelland 1994).Due to its conjunctive information processing after receiving inputs from multiple sources (e.g., information for object recognition, egocentric memory, allocentric memory, etc.), the hippocampal system is prone to competition with other systems especially when a simpler strategy that requires information from a single source seems a viable option. Behavioral and pharmacological studies have supported this hypothesis (Packard and McGaugh 1996;Poldrack and Packard 2003). Physiologically, the influence of switching strategy on hippocampal ne...

Still searching for the engram

“…By contrast, in the “place”-strategy variant, regardless of whether they began in the North or South arms, they were required to enter the East arm to find reward. 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).…”

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

“…During the initial training sessions on the OPPA task, rats exhibit a “side bias” for selecting the object over a well on a particular side, regardless of the object or the arm of the maze (Hernandez et al, 2015; Jo and Lee, 2010a; Lee and Byeon, 2014; Lee and Kim, 2010). This bias has to be suppressed, presumably through mPFC activity projecting back to sensorimotor areas (Lee and Byeon, 2014) before OPPA task performance shows an improvement.…”

Hippocampus is required for paired associate memory with neither delay nor trial uniqueness

“…The paired associate memory paradigm has been extensively used in human and animal models for its known dependence on the hippocampus Eichenbaum 1993, 1996;Cho and Kesner 1995;Vargha-Khadem et al 1997;Gilbert and Kesner 2002;Day et al 2003;Kesner et al 2005;Tse et al 2007;Hannula and Ranganath 2008;Solivan 2008, 2010;Holdstock et al 2010;Lee and Kim 2010). A one-trial delayed-cued retrieval task for paired associate memory (Day et al 2003;Kesner et al 2008) may certainly contribute to the investigation of the role of hippocampus in episodic-like memory in animals.…”