Development of the Hippocampal Cognitive Map in Preweanling Rats

By Thomas J. Wills, F. Cacucci, Neil Burgess, John O'Keefe. 2010

591 citations recorded by the source corpus.

The Space in Your Head Space, and events associated with places and spaces, are represented in the brain by a circuitry made of place cells, head direction cells, grid cells, and border cells. These cell types form a collective dynamic representation of our position as we move through the environment. How this representation is formed has remained a mystery. Is it acquired, or are we born with the ability to represent external space (see the Perspective by Palmer and Lynch)? Langston et al. (p. 1576) and Wills et al. (p. 1573) investigated the early development of spatial activity in the hippocampal formation and the entorhinal cortex of rat pups when they first began to explore their environment. Rudiments of place cells, head direction cells, and grid cells already existed when the pups made their first movements out of the nest. A neural representation of external space at this early time points to strong innate components for perception of space. These findings provide experimental support for Kant's 200-year-old concept of space as an a priori faculty of the mind. Some aspects of spatial cognition develop very early and may be determined innately. Orienting in large-scale space depends on the interaction of environmental experience and preconfigured, possibly innate, constructs. Place, head-direction, and grid cells in the hippocampal formation provide allocentric representations of space. Here we show how these cognitive representations emerge and develop as rat pups first begin to explore their environment. Directional, locational, and rhythmic organization of firing are present during initial exploration, including adultlike directional firing. The stability and precision of place cell firing continue to develop throughout juvenility. Stable grid cell firing appears later but matures rapidly to adult levels. Our results demonstrate the presence of three neuronal representations of space before extensive experience and show how they develop with age.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

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Citations in the corpus

CA3 Retrieves Coherent Representations from Degraded Input: Direct Evidence for CA3 Pattern Completion and Dentate Gyrus Pattern Separation (2014, background): “…2011); (2) during development, adult-like place field firing patterns appear before well-formed grid-cell firing patterns (Langston et al., 2010; Wills et al., 2010); (3) cue-card manipulations in a cylindrical environment can cause discordant responses of grid cells and place cells (Song et…”
Generative Predictive Codes by Multiplexed Hippocampal Neuronal Tuplets. (2018, unknown): “10 Neuron 99, 1–13, September 19, 2018 appear quantal, continuous, and sequential in nature and have been proposed to conceptually emerge a priori, before explicit experience (Kant, 1781; Langston et al., 2010; Wills et al., 2010).”
The neuroscience of learning: beyond the Hebbian synapse. (2013, background): “These cells are present in rudimentary form as soon as rat pups leave the nest (Langston et al. 2010, Wills et al. 2010), suggesting important genetic control over their development, that is, a genetic basis for the mechanisms by which the brain represents experienced spatial geometry.”
Attractor and integrator networks in the brain (2021, background): “These considerations suggest a hypothesis for circuits with  2-D continuous attractors: Evolutionarily conserved circuits that do not require extensive early experience [276, 277] should be topographically organized.”
Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planning (2015, background): “The constructive or anterograde role of SPW-Rs is also expected from the early presence of SPWs in ontogenetic development (see Development of Sharp Waves and Ripples section), before the emergence of hippocampal place cells and entorhinal grid cells (Wills et al., 2010; Langston et al., 2010).”
A model of grid cell development through spatial exploration and spike time-dependent plasticity. (2014, unknown): “I I -45 -12 30 0 80 0 80 200 0 neuron 200 80 0 80 0 0 200 0 0 80 80 0 neuron neuron 100 0 200 0 neuron neuron 0 10 20 200 0”
Interactive specialization: a domain-general framework for human functional brain development? (2011, unknown): “…M.H. Johnson / Developmental words, some cortical regions become more specialized with development.3 This process mirrors that known to occur at a cellular level during development, in which receptive or activity fields become increasingly fine-grained during development (e.g. Wills et al., 2010).”
Design Principles of the Hippocampal Cognitive Map (2014, background): “Fist, recent evidence suggests that the emergence of place cells does not depend on grid cell input [4, 47].”