Information encoding by means of persistent changes in synaptic strength supports long-term information storage and memory in structures such as the hippocampus. In the piriform cortex (PC), that engages in the processing of associative memory, only short-term synaptic plasticity has been described to date, both in vitro and in anesthetized rodents in vivo. Whether the PC maintains changes in synaptic strength for longer periods of time is unknown: Such a property would indicate that it can serve as a repository for long-term memories. Here, we report that in freely behaving animals, frequency-dependent synaptic plasticity does not occur in the anterior PC (aPC) following patterned stimulation of the olfactory bulb (OB). Naris closure changed action potential properties of aPC neurons and enabled expression of long-term potentiation (LTP) by OB stimulation, indicating that an intrinsic ability to express synaptic plasticity is present. Odor discrimination and categorization in the aPC is supported by descending inputs from the orbitofrontal cortex (OFC). Here, OFC stimulation resulted in LTP (>4 h), suggesting that this structure plays an important role in promoting information encoding through synaptic plasticity in the aPC. These persistent changes in synaptic strength are likely to comprise a means through which long-term memories are encoded and/or retained in the PC.

Whereas the postrhinal cortex (POR) is a critical center for the integration of egocentric and allocentric spatial information, the perirhinal cortex (PRC) plays an important role in the encoding of objects that supports spatial learning. The POR and PRC send afferents to the hippocampus, a structure that builds complex associative memories from the spatial experience. Hippocampal encoding of item-place experience is accompanied by the nuclear expression of immediate early gene (IEGs). Subfields of the Cornus ammonius and subregions of the hippocampus exhibit differentiated and distinct encoding responses, depending on whether the spatial location and relationships of large highly visible items (macroscale encoding) or small partially concealed items (microscale encoding), is learned. But to what extent the PRC and POR support hippocampal processing of different kinds of item-place representations is unclear. Using fluorescence in situ hybridization (FISH), we examined the effect of macroscale (overt, landmark) and microscale (subtle, discrete) item-place learning on the nuclear expression of the IEG, Arc. We observed an increase in Arc mRNA in the caudal part of PRC area 35 and the caudal part of the POR after macroscale, but not microscale item-place learning. The caudal part of PRC area 36, the rostral and middle parts of PRC areas 35 and 36, as well as the middle part of the POR responded to neither type of item. These results suggest that macroscale items may contain a strong identity component that is processed by specific compartments of the PRC and POR. In contrast small, microscale items are not encoded by the POR or PRC, indicating that item dimensions may play a role in the involvement of these structures in item processing.

The hippocampus utilizes olfactospatial information to encode sensory experience by means of synaptic plasticity. Odor exposure is also a potent impetus for hippocampus-dependent memory retrieval. Here, we explored to what extent the piriform cortex directly impacts upon hippocampal information processing and storage. In behaving rats, test-pulse stimulation of the anterior piriform cortex (aPC) evoked field potentials in the dentate gyrus (DG). Patterned stimulation of the aPC triggered both long-term potentiation (LTP > 24 h) and short-term depression (STD), in a frequency-dependent manner. Dual stimulation of the aPC and perforant path demonstrated subordination of the aPC response, which was nonetheless completely distinct in profile to perforant path-induced DG plasticity. Correspondingly, patterned aPC stimulation resulted in somatic immediate early gene expression in the DG that did not overlap with responses elicited by perforant path stimulation. Our results support that the piriform cortex engages in specific control of hippocampal information processing and encoding. This process may underlie the unique role of olfactory cues in information encoding and retrieval of hippocampus-dependent associative memories.

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The perirhinal cortex (PRC), subdivided into areas 35 and 36, belongs to the parahippocampal regions that provide polysensory input to the hippocampus. Efferent and afferent connections along its rostro-caudal axis, and of areas 35 and 36, are extremely diverse. Correspondingly functional tasks in which the PRC participates are manifold. The PRC engages, for example, in sensory information processing, object recognition, and attentional processes. It was previously reported that layer II of the caudal area 35 may be critically involved in the encoding of large-scale objects. In the present study we aimed to disambiguate the roles of the different PRC layers, along with areas 35 and 36, and the rostro-caudal compartments of the PRC, in processing information about objects of different dimensions. Here, we compared effects on information encoding triggered by learning about subtle and discretely visible (microscale) object information and overt, highly visible landmark (macroscale) information. To this end, nuclear expression of the immediate early gene Arc was evaluated using fluorescence in situ hybridization. Increased nuclear Arc expression occurred in layers III and V-VI of the middle and caudal parts of area 35 in response to both novel microscale and macroscale object exposure. By contrast, a significant increase in Arc expression occurred in area 36 only in response to microscale objects. These results indicate that area 36 is specifically involved in the encoding of small and less prominently visible items. In contrast, area 35 engages globally (layer III to VI) in the encoding of object information independent of item dimensions.