A mechanism for the formation of hippocampal neuronal firing patterns that represent what happens where

Abstract

The association of specific events with the context in which they occur is a fundamental feature of episodic memory. However, the underlying network mechanisms generating what-where associations are poorly understood. Recently we reported that some hippocampal principal neurons develop representations of specific events occurring in particular locations (item-position cells). Here, we investigate the emergence of item-position selectivity as rats learn new associations for reward and find that before the animal's performance rises above chance in the task, neurons that will later become itemposition cells have a strong selective bias toward one of two behavioral responses, which the animal will subsequently make to that stimulus. This response bias results in an asymmetry of neural activity on correct and error trials that could drive the emergence of particular item specificities based on a simple reward-driven synaptic plasticity mechanism.The hippocampus is critically involved in the acquisition of new episodic memories (Scoville and Milner 1957;Eichenbaum 2000). In particular, the formation of associations between events and the context where they occur, a fundamental feature of episodic memory, depends on hippocampal function (Manns and Eichenbaum 2006;Eichenbaum et al. 2007).We have recently shown that some hippocampal principal neurons develop representations of specific events occurring in particular locations (Komorowski et al. 2009). In this study, animals learned which of two stimulus items (what) was rewarded depending on the environmental context (where) in which the items were presented (Rajji et al. 2006;Manns and Eichenbaum 2009). On each trial, a rat initially explored one of the two contexts, after which the two stimulus items were placed into different positions (corners) of the context (Fig. 1A); the animal then investigated the items (scented flower pots), and should learn to dig (Go response) for a buried food reward in the appropriate pot for that context or not dig (NoGo) at pots where no reward was buried. All animals performed at no better than chance (50%) for the first 30 trials, then acquired the what-where associations, reaching an average accuracy of 86% in the last 30 trials of the training session (Fig. 1B).In this paradigm, we previously indentified principal neurons showing differential firing during the sampling of one of the two stimulus items when located in the same position (Fig. 1C, left), which we called as item-position (IP) cells (Komorowski et al. 2009). IP cell responses did not distinguish the items during the first 30 trials of the learning session, but did fire during item sampling at particular locations. Subsequently, we showed that many IP cells increased firing during the sampling of an item-position combination in parallel with learning (Fig. 1C, left). Importantly, we observed approximately equivalent selectivity for rewarded and nonrewarded item-position combinations (Fig. 1C, middle). We also identified principal neurons that were active during item sampl...

The influence of low-level stimulus features on the representation of contexts, items, and their mnemonic associations

“…We built upon a well-designed approach used in the rodent (Rajji et al, 2006; Komorowski et al, 2009, 2013; Navawongse and Eichenbaum, 2013; Tort et al, 2013; McKenzie et al, 2014; Farovik et al, 2015; Keene et al, 2016) and observed many analogous patterns using fMRI in humans. However, the results of our experiments highlight the importance of controlling for low-level sensory differences between the experimental conditions—here, different contexts and objects.…”

“…In a series of groundbreaking studies, Eichenbaum and colleagues used a context-guided object association task to explore how the components of an associative memory such as context, item, position, and valance are represented neurally (Rajji et al, 2006; Komorowski et al, 2009, 2013; Navawongse and Eichenbaum, 2013; Tort et al, 2013; McKenzie et al, 2014; Farovik et al, 2015; Keene et al, 2016). Briefly, animals learn item-reward associations that differ based on the context, which was operationally defined as visually, tactilely, and spatially (side of the apparatus) distinct chambers.…”

“…Additionally, we investigated representations in retrosplenial cortex (RSC), a subregion of the posterior cingulate cortex (PCC), which has been hypothesized to be involved in processing scenes and contexts (Chen et al, 1994; Ennaceur et al, 1997; Cho and Sharp, 2001; Vann and Aggleton, 2002; Bar and Aminoff, 2003; Parron and Save, 2004; Park and Chun, 2009; Walther et al, 2009; Auger and Maguire, 2013; Alexander and Nitz, 2015; Auger et al, 2015; Wing et al, 2015) in addition to playing a role in declarative memory, spatial memory, and the formation of stimulus-stimulus associations (Valenstein et al, 1987; Vann et al, 2009; Aggleton, 2010; Ranganath and Ritchey, 2012; Bucci and Robinson, 2014). In Experiment 1, we used distinct stimuli for our contexts and objects, similar to the rodent studies (Rajji et al, 2006; Komorowski et al, 2009, 2013; Navawongse and Eichenbaum, 2013; Tort et al, 2013; McKenzie et al, 2014; Farovik et al, 2015; Keene et al, 2016). In Experiment 2, we matched the low-level visual features of our stimulus set to test for context and object representation in the absence of the confounding effect of low-level sensory differences between stimuli.…”

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

“…According to this view, ensembles pattern-separate similar stimuli during learning when rewards depend upon discriminating previously neutral stimuli (e.g. Tort et al, 2011). The increased pattern separation may reflect the emergence of a new organization of information.…”

Effects of odor on emotion, with implications

“…Hippocampal damage impairs odor-place associative learning, and temporal order memory for odor information (Kesner et al, 2002; Rolls and Kesner, 2006). Some neurons in the hippocampus represent the place of odor-related reward (Rolls, 2010; Tort et al, 2011). In addition, stimulation of the hippocampus affects autonomic responses, that is, decreases heart rate and blood pressure (Ruit and Neafsey, 1988).…”