Orchestration of Hippocampal Information Encoding by the Piriform Cortex

Abstract

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.

Odour-Evoked Memory in Dogs: Do Odours Help to Retrieve Memories of Food Location?

“…Furthermore, recent studies in behaving rats have also suggested a fundamental role of the piriform cortex in modulating the functioning of the neural network between the olfaction and the hippocampus. Specifically, the work of Strauch and Manahan-Vaughan [ 49 ] provides evidence that activity in the piriform cortex evokes field potentials in the dentatus gyrus supporting the hypothesis about the main role of the piriform cortex in specific control of hippocampal information processing and encoding. The piriform cortex represents the largest domain of the olfactory cortex playing a pivotal role of olfactory information processing because its neural network connections with all parts of the lateral entorhinal cortex [ 52 , 53 ].…”

“…The existence of a unique association between an odor and the spatial information (i.e., reward location) created during the encoding phase is further supported by the relationship between olfaction and the neural structures involved in several cognitive processes, including memory, emotions, and associative learning [ 21 ]. In particular, exclusive anatomical connections between the olfactory cortex and the hippocampus suggest that this neural circuit could be the main involved during contextually odor cued spatial memory recall tests [ 49 , 50 ]. The hippocampus in fact, is crucial for spatiotemporal context representation and its association with the sensory details, which come from the environment to form episodic memories [ 50 , 51 ].…”

“…The latter drives unimodal sensory information along with attentional and motivational information conveyed by the anterior brain regions to the hippocampus. On the other hand, behavioral, anatomical and electrophysiological evidences support a role for the dentate gyrus, which appears to be largely sensitive to olfactory stimuli, in mnemonic processing of spatial information [ 49 , 54 ].…”

Cell Proliferation in the Piriform Cortex of Rats with Motor Cortex Ablation Treated with Growth Hormone and Rehabilitation

“…The PC is the area of the brain that receives the most afferent connections from the olfactory bulb. The PC establishes efferent connections with a large number of brain areas: olfactory structures (primary olfactory cortex, pedicle cortex, amygdala, olfactory tubercle), the limbic system (thalamus and hypothalamus), the entorhinal cortex [ 63 , 64 ], the prefrontal cortex [ 65 ] and with the superior colliculus [ 66 ]. It also establishes important ipsilateral and reciprocal connections with the orbitofrontal cortex, which is a higher integrative center that encodes olfactory information and determines the significance of these stimuli, modulating behavior in response to them [ 67 ].…”

RGS14 modulates locomotor behavior and ERK signaling induced by environmental novelty and cocaine within discrete limbic structures

“…Though the behavioral functions of CA2 have been studied mostly in the context of social memory (Dudek et al 2016; Hitti and Siegelbaum 2014; Meira et al 2018), the remaining RGS14-ir regions have established roles in spatial memory (McDonald and White 2013), novelty detection (Moreno-Castilla et al 2017; Strauch and Manahan-Vaughan 2020), motivation (Baker et al 2002), and behavioral responses to stress or psychostimulants (Fadok et al 2018; Kabbaj et al 2000). The expression pattern of RGS14 throughout these distributed brain regions, all of which receive glutamatergic and DAergic innervation (Datiche and Cattarelli 1996; Fadok et al 2018; McNamara and Dupret 2017; Takeuchi et al 2016), guided our decision to assess unconditioned behavioral responses to novelty and psychostimulants in RGS14 KO mice, which to date have been almost exclusively examined in behavioral paradigms that assess learning and memory.…”