Perirhinal cortex is necessary for acquiring, but not for retrieving object–place paired association

Abstract

Remembering events frequently involves associating objects and their associated locations in space, and it has been implicated that the areas associated with the hippocampus are important in this function. The current study examined the role of the perirhinal cortex in retrieving familiar object-place paired associates, as well as in acquiring novel ones. Rats were required to visit one of two locations of a radial-arm maze and choose one of the objects (from a pair of different toy objects) exclusively associated with a given arm. Excitotoxic lesions of the perirhinal cortex initially impaired the normal retrieval of object-place paired-associative memories that had been learned presurgically, but the animals relearned gradually to the level of controls. In contrast, when required to associate a novel pair of objects with the same locations of the maze, the same lesioned rats were severely impaired with minimal learning, if any, taking place throughout an extensive testing period. However, the lesioned rats were normal in discriminating two different objects presented in a fixed arm in the maze. The results suggest that the perirhinal cortex is indispensable to forming discrete representations for object-place paired associates. Its role, however, may be compensated for by other structures when familiar object-place paired associative memories need to be retrieved.Remembering an event in space often requires associating objects and their locations. Associating object and place information into a unitary event representation is believed to be a foundation of episodic memory (Cahusac et al. 1989;Gaffan 1994;Davachi 2006). It has been suggested that the hippocampus and its associated regions in the medial temporal lobe (MTL) are essential in this cognitive process, and amnesic patients with damage in the MTL structures exhibit severe deficits in associating object and place information (Smith and Milner 1981;Vargha-Khadem et al. 1997;Stepankova et al. 2004). Animal models produced by localized lesions in the hippocampus and other MTL structures also support the idea by showing that the lesioned animals are impaired in associating objects and places (Parkinson et al. 1988;Gaffan and Parker 1996;Sziklas et al. 1998;Bussey et al. 2001; Kesner 2003, 2004;Malkova and Mishkin 2003;Lee et al. 2005;Bachevalier and Nemanic 2008;Kesner et al. 2008;Lee and Solivan 2008). Although the theoretical importance of the MTL structures in object-place association has been well acknowledged, specific contributions of the MTL structures in object-place associative memory are poorly understood. The current study examined the role of the perirhinal cortex, one of the extra hippocampal regions in the MTL, using a behavioral paradigm previously shown to be dependent on the intact hippocampus (Lee and Solivan 2008).The literature suggests that the role of the hippocampus in the object-place paired-associate task is to put together object and place information into a unified and distinct event representation. It has been suggested that spa...

Age-related impairments in object-place associations are not due to hippocampal dysfunction.

“…The dissociation of deficits in acquisition of object-place associations versus intact spatial reference memory in aged animals provides important insights with regards to aging. Lesion data have shown that the prefrontal cortex (PFC; Lee & Solivan, 2008) and the perirhinal cortex (PER; Jo & Lee, 2010a, 2010b) are both necessary for OPPA task, but not water maze, performance (Machin, Vann, Muir, & Aggleton, 2002; Sloan et al, 2006). Thus, these data support the hypothesis that age-associated disruptions in the PER (Burke et al, 2012; Burke et al, 2014) and/or PFC (Banuelos et al, 2014; Barense et al, 2002) are likely contributing to the performance deficits of aged animals on the OPPA task.…”

“…These data suggest that quantifying an animal’s ability to form and retain object-place associations across the life span could provide insight regarding memory network interactions in advanced age. In the current experiment, young and aged rats were monitored while they performed the object-place paired association task (OPPA; Jo & Lee, 2010a), which is believed to require HPC-PER-PFC interactions (Jo & Lee, 2010a, 2010b; Lee & Solivan, 2008). Individual aged rats with intact performance on the Morris water maze test of spatial reference memory (Morris, 1984) were significantly impaired on the OPPA task.…”

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

“…Rats often display response biases during the acquisition of the OPPA task prior to learning the object-in-place rule (Hernandez et al, 2015; Jo and Lee, 2010a; b; Lee and Byeon, 2014). Thus, indices of a side bias (left vs. right well) and object bias (e.g.…”

“…Although the mPFC is necessary for an animal’s ability to inhibit an incorrect response (Lee and Byeon, 2014; Lee and Solivan, 2008), and mPFC-PER communication is involved in an animal’s ability to detect novel object-place associations (Barker et al, 2007; Barker and Warburton, 2008; 2015; Jo and Lee, 2010a; b), it is not known if communication between these brain areas is critical for flexible behavior. The objective of the current experiments was to examine whether mPFC-PER communication is necessary for performance on the object-place paired association (OPPA) task (Jo and Lee, 2010b), which tests an animal’s ability to flexibly update which of two objects is rewarded based on an incrementally learned object-in-place rule that requires knowledge of both object identity and current spatial location.…”

“…The objective of the current experiments was to examine whether mPFC-PER communication is necessary for performance on the object-place paired association (OPPA) task (Jo and Lee, 2010b), which tests an animal’s ability to flexibly update which of two objects is rewarded based on an incrementally learned object-in-place rule that requires knowledge of both object identity and current spatial location. After rats acquired the biconditional association, the necessity of mPFC-PER communication was investigated by infusing the GABA A receptor agonist muscimol (MUS) into one hemisphere of the mPFC and the contralateral PER to reversibly disconnect these areas.…”