Cognitive maps beyond the hippocampus

Abstract

We present a conceptual framework for the role of the hippocampus and its afferent and efferent structures in rodent navigation. Our proposal is compatible with the behavioral, neurophysiological, anatomical, and neuropharmacological literature, and suggests a number of practical experiments that could support or refute it. We begin with a review of place cells and how the place code for an environment might be aligned with sensory cues and updated by self‐motion information. The existence of place fields in the dark suggests that location information is maintained by path integration, which requires an internal representation of direction of motion. This leads to a consideration of the organization of the rodent head direction system, and thence into a discussion of the computational structure and anatomical locus of the path integrator. If the place code is used in navigation, there must be a mechanism for selecting an action based on this information. We review evidence that the nucleus accumbens subserves this function. From there, we move to interactions between the hippocampal system and the environment, emphasizing mechanisms for learning novel environments and for aligning the various subsystems upon re‐entry into familiar environments. We conclude with a discussion of the relationship between navigation and declarative memory. Hippocampus 7:15–35, 1997. © 1997 Wiley‐Liss, Inc.

Age-related deficits in the ability to encode contextual change: A place cell analysis

“…This conclusion is further supported by recent preliminary reports showing that place cells respond differentially, dependent on the trajectory to be executed (Frank and Wilson, 1999;Wood et al, 1999). The present data support the hypothesis that hippocampal units encode location within a given reference frame or context (Redish and Touretzky, 1997;Redish, 1999). Consequently, in addition to representing many different environments, the hippocampus can provide multiple representations of a given environment, a mechanism well suited to underlie episodic memory.…”

Spatial cognition and neuro-mimetic navigation: a model of hippocampal place cell activity

“…In particular, we consider the output of CA1 cells that reaches the nucleus accumbens via the fornix 1 . We identify the NA as the area in which navigation control is achieved by means of reward-based learning (Brown and Sharp 1995;Redish and Touretzky 1997). We consider the dopaminergic input that NA receives from the ventral tegmental area (VTA).…”

“…The hippocampal formation consists of the hippocampus proper, the dentate gyrus, the entorhinal cortex, and the subicular complex (Redish 1997;Burgess et al 1999). Adapted from Redish and Touretzky (1997), and from Burgess et al (1999) 2.2 Learning place ®elds…”

“…Our approach is similar in spirit to earlier studies (Burgess et al 1994;Brown and Sharp 1995;Gaussier et al 1997;Mallot et al 1997;Redish 1997;Redish and Touretzky 1997;Trullier and Meyer 1997). In contrast to Burgess et al (1994), we do not directly use metric information (i.e., distance to visual cues) as input for the model.…”

“…This allows us to account for the existence of place ®elds in the absence of visual cues (e.g., in complete darkness) (Quirk et al 1990). Redish and Touretzky (Redish 1997;Redish and Touretzky 1997) have put forward a comprehensive theory of the hippocampal functionality where place ®elds are important ingredients. Our approach puts the focus on how place ®elds in the CA3-CA1 areas might be built from multimodal sensory inputs (i.e., vision and path integration).…”