The global record of memory in hippocampal neuronal activity

Abstract

In humans the hippocampal region of the brain is crucial for declarative or episodic memory for a broad range of materials. In contrast, there has been controversy over whether the hippocampus mediates a similarly general memory function in other species, or whether it is dedicated to spatial memory processing. Evidence for the spatial view is derived principally from the observations of 'place cells'-hippocampal neurons that fire whenever the animal is in a particular location in its environment, or when it perceives a specific stimulus or performs a specific behaviour in a particular place. We trained rats to perform the same recognition memory task in several distinct locations in a rich spatial environment and found that the activity of many hippocampal neurons was related consistently to perceptual, behavioural or cognitive events, regardless of the location where these events occurred. These results indicate that nonspatial events are fundamental elements of hippocampal representation, and support the view that, across species, the hippocampus has a broad role in information processing associated with memory.

The hippocampal debate: are we asking the right questions?

“…A key question becomes whether the spatial and non-spatial correlations are equivalent or not. Memory theories suggest that they are equivalent [4,33,46,246], while spatial theories suggest that nonspatial variables are second-order effects [177,196,225], or even deny their existence [147]. What I am proposing here is that spatial and non-spatial correlations are both important, that they follow from similar processes, but that they show very different properties.…”

“…Those of us who have come into the field long after the acceptance of place cells can only imagine the surprise and disbelief that accompanied their initial discovery [14,142]. Although no one denies that under certain conditions, hippocampal pyramidal cells show spatial tuning curves (place fields), even today there are authors who argue that, dramatic though they may be, place fields are epiphenomena, a consequence of the spatial nature of experimental design [46,71,142,246].…”

“…By this point, it is pretty much accepted that under certain conditions, hippocampal pyramidal cells show correlations to non-spatial aspects [48,69,71,101,109,157,238,239,246,247,250] (see [33,173] for reviews, but see [147] for an alternative viewpoint). These non-spatial aspects include when animals change task within an environment [101], in response to components of a task in which goals change [48,69,157,247], even after salient events [202].…”

“…All non-spatial hippocampal correlates have been measured along categorized dimensions: specific odors [48,246], whether a cue is black or white [17], whether the goal is to the left or right of a T-maze [54,247], whether a lever is to the left or to the right [71], whether two sequential cues match or not [69,157,[193][194][195], which behavior is to be elicited [101], etc. In contrast, studies of spatial dimensions have shown conclusively that the representation changes continuously (e.g.…”

Conjoint Control of Hippocampal Place Cell Firing by Two Visual Stimuli

“…We therefore chose to develop a numerical theory that emphasizes the global control of all cells by each identified stimulus. Our choice of such a model reflects our belief that the place-cell population represents a large scale, unitary construct, the environment, rather than an agglomeration of separate, smaller-scale features of the environment such as pairwise relationships between objects (O'Keefe and Conway 1978; Hetherington and Shapiro 1997; but see Shapiro et al 1997; Wood et al 1999). In part, this view is based on the notion that place cells (especially CA3 place cells) interact with each other and are not a set of independent feature detectors (Muller et al 1991, Muller et al 1996; Blum and Abbott 1996; Mehta et al 1997; Samsonovich and McNaughton 1997).…”