Neural Correlates of Object-Associated Choice Behavior in the Perirhinal Cortex of Rats

Abstract

The perirhinal cortex (PRC) is reportedly important for object recognition memory, with supporting physiological evidence obtained largely from primate studies. Whether neurons in the rodent PRC also exhibit similar physiological correlates of object recognition, however, remains to be determined. We recorded single units from the PRC in a PRC-dependent, object-cued spatial choice task in which, when cued by an object image, the rat chose the associated spatial target from two identical discs appearing on a touchscreen monitor. The firing rates of PRC neurons were significantly modulated by critical events in the task, such as object sampling and choice response. Neuronal firing in the PRC was correlated primarily with the conjunctive relationships between an object and its associated choice response, although some neurons also responded to the choice response alone. However, we rarely observed a PRC neuron that represented a specific object exclusively regardless of spatial response in rats, although the neurons were influenced by the perceptual ambiguity of the object at the population level. Some PRC neurons fired maximally after a choice response, and this post-choice feedback signal significantly enhanced the neuronal specificity for the choice response in the subsequent trial. Our findings suggest that neurons in the rat PRC may not participate exclusively in object recognition memory but that their activity may be more dynamically modulated in conjunction with other variables, such as choice response and its outcomes.

Complementary Functional Organization of Neuronal Activity Patterns in the Perirhinal, Lateral Entorhinal, and Medial Entorhinal Cortices

“…Both studies provided evidence of spatial "memory" fields at prior locations when objects were moved in or removed from the environment, whereas Deshmukh et al (2011) also provided examples of activity similar to place field firing when objects were presented. In addition, studies on earlier stages of information processing before LEC and MEC (i.e., in the PRC and postrhinal cortex) have also reported mixed selectivity of neuronal activity in animals performing memory tasks where objects and spatial choices are relevant (Furtak et al, 2012;Ahn and Lee, 2015). The present findings suggest that both LEC and MEC also represent organizations of objects and events within spatial contexts (see also and that even PRC exhibits a combination of object and spatial coding.…”

“…By contrast, LEC neurons exhibit little spatial specificity in this behavioral situation (Hargreaves et al, 2005) and PRC neurons exhibit none (Deshmukh et al, 2012). Conversely, in experiments where animals perform object recognition or discrimination tasks, PRC and LEC neurons fire during the presentation of specific odor (in rats) or visual (in monkeys) cues, during maintenance of nonspatial memories, or associated with behavioral responses, but firing patterns associated with the animals' location in space were not examined (Suzuki et al, 1997;Young et al, 1997;Yanike et al, 2009;Igarashi et al, 2014;Ahn and Lee, 2015;Brown and Banks, 2015). Some recent studies have identified activity in PRC and LEC neurons associated with objects or visual patterns in particular places as animals explore an open field (Deshmukh and Knierim, 2011;Deshmukh et al, 2012;Tsao et al, 2013) or traverse a circular path in a maze (Burke et al, 2012;Neunuebel et al, 2013).…”

Representation of memories in the cortical–hippocampal system: Results from the application of population similarity analyses

“…In the three areas, representations of identical events are most closely associated (correlation of odd/even trials). Thus, although PRC, LEC and MEC exhibit similarity in mixed selectivity at the single neuron level, RSA reveals that information is organized in distinct but complementary ways (see also Ahn and Lee, 2015; Beer et al, 2013; Deshmukh and Knierim, 2011; Ohyama et al, 2012). …”

Rodent age‐related impairments in discriminating perceptually similar objects parallel those observed in humans

“…While age‐related dysfunction within hippocampal circuits is well‐documented (Burke & Barnes, ; Burke & Barnes, ; Rosenzweig & Barnes, ; Wilson, Gallagher, Eichenbaum, & Tanila, ), the emergence of disrupted function across cortical subregions of the medial temporal lobe has not been fully examined. Thus, despite the established importance of perirhinal cortex in forming high‐order sensory representations and discriminating between them (Ahn & Lee, ; Bartko, Winters, Cowell, Saksida, & Bussey, ,b; Byun & Lee, ; Graham, Barense, & Lee, ), the contribution of change in neural communication across these circuits to age‐related discrimination deficits remains unknown.…”

“…Both animal and human studies have reported declines in stimulus discrimination abilities with age, yet distinct potential mechanisms have been highlighted between different species. The ability to discriminate between similar objects has been shown to require the perirhinal cortex in rats (Ahn & Lee, ; Bartko et al, ; Eacott, Machin, & Gaffan, ; Winters, Bartko, Saksida, & Bussey, ; Hales, Broadbent, Velu, Squire, & Clark, ) and monkeys (Baxter & Murray, ; Buckley & Gaffan, ; Bussey, Saksida, & Murray, ). On the other hand, the majority of neuroimaging studies that have directly investigated object discrimination abilities in humans have shown a consistent relationship between task performance and activation within the CA3/dentate gyrus circuit (Bakker, Albert, Krauss, Speck, & Gallagher, ; Bakker, Kirwan, Miller, & Stark, ; Bakker et al, ; Doxey & Kirwan, ; Kirwan & Stark, ; Lacy, Yassa, Stark, Muftuler, & Stark, ; Motley & Kirwan, ; Reagh & Yassa, ; Yassa et al, , Yassa, Mattfeld, Stark, & Stark, ).…”