Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Spatial Orientation

Science 18 June 2010: Vol. 328. no. 5985, pp. 1487 - 1488

Neuroscience: A Kantian View of Space

Linda Palmer and Gary Lynch

Department of Anatomy and Neurobiology, University of California, Irvine, CA 92697, USA.




























How does the brain represent space? Is this representation entirely the result of learning from experience? Two scientific studies report that critical components of the brain's spatial representation systems are already in place when an animal first encounters an extended environment. This supports the view that spatial representation indeed includes an innate component prior to experience.

In both studies, the researchers placed electrodes in the hippocampal formation of freely moving 14-day-old rat pups (a remarkable technical achievement), and recorded the activity ("firing" of electrical impulses) of individual neurons at 16 days after birth and up to 2 weeks afterward. They were thus able to sample three classes of cells with distinctly different spatial coding characteristics when the pups leave their nest to first explore the outside world (see the figure). The studies agree that two of these cell types—one that discharges when the animal's head points in a particular direction relative to the environment ("direction cells") and a second that fires when the rat moves through a particular location within the environment ("place cells") —are present at day 16, only 2 days after the eyes have opened. Both studies indicate that the direction cells in the rat pups are already adultlike, whereas the place cells increase in number and undergo considerable refinement with age and experience.

The studies also discuss  A third class of spatial neurons. These "grid cells" fire in repeated discrete locations as the animal moves around its environment, forming the vertices of a polygonal grid that covers the environment.

The results for place and grid neurons raise the question of the role of learning, as opposed to the onset of preformed neuronal network operations, in the emergence of these cell types during first exploration of an environment. Both studies address this issue by testing animals at different ages in unfamiliar surroundings, reasoning that older first explorers will have more adultlike cells if maturation plays the dominant role. This was the case: The number of neurons encoded to location increased steadily as a function of the age at first exposure, rather than number of exposures.

Long-term potentiation, a form of synaptic plasticity associated with memory formation, appears in the hippocampus by age 11 days in rats and then undergoes a maturation that extends through the third week after birth. Direction, place, and grid cells in adults predominate (for the most part) in different regions of the brain. Both reports describe compelling evidence that the three types of neuronal activity observed predominate in their appropriate subdivisions in the youngest rats tested.

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Development of the Hippocampal Cognitive Map in Preweanling Rats

Tom J. Wills,1 Francesca Cacucci,1,2 Neil Burgess,3,4 John O'Keefe1

1 Cell and Developmental Biology, University College London, Gower Street, London WC1E 6BT, UK.
2 UC Institute of Behavioural Neuroscience, Division of Psychology and Language Sciences, University College London, London WC1H 0AP, UK.
3 UC Institute of Cognitive Neuroscience, University College London, London WC1N 3AR, UK.
4 UC Institute of Neurology, University College London, London WC1N 3BG, UK.


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.

The hippocampal cognitive map has been proposed as a Kantian synthetic a priori system, partly or wholly formed genetically, to serve as a scaffold for representing experiential information about the external environment. This suggests that the basic constituents of the cognitive map develop independently of spatial experience, or might even precede it, and is supported by the early development of spatial cognition in weanling rats. We tested this idea by looking for place cells in hippocampal region CA1, and for grid and directional cells in medial entorhinal cortex (MEC) as preweanling rats first began to leave the nest and to actively explore their environment [typically on postnatal day 16 (P16) in our experiment].

We recorded 567 hippocampal pyramidal cells and 1514 medial entorhinal cells from 42 male rats between the ages of P16 and P30 as they foraged for food in an enclosure, using miniaturized microdrives and recording locations matched across ages. Cells were categorized as directional, place, or grid cells if their spatial firing characteristics exceeded the 0.05 significance level of the relevant measures [spatial information for place cells, gridness for grid cells, Rayleigh vector for directional cells] in spatially shuffled data for the corresponding age and region.

In adult rats, the firing of place and grid cells is carefully timed to the theta rhythm ["phase precession"], and theta oscillations may play a role in the creation of place and grid firing. Theta frequency increased with age and with running speed [as in adults]. Theta amplitude showed a similar profile. Both the slope and intercept of the frequency-speed relation increased with age. Finally, the frequency of modulation (indicated by the power spectrum of the spike-train autocorrelogram) of grid and place cell firing was slightly higher than the simultaneously recorded local field potential theta; this finding is consistent with the presence of phase precession.

Our results have general implications for the interaction of innate and experientially acquired knowledge in spatial cognition. The expression of some types of spatial learning ability continues to improve for a long time after the components of the cognitive map are relatively mature. Some types of spatial behavior in rats, such as spatial orientation based on enclosure geometry, are likely directly controlled by head-direction cells, so that our evidence for an early, perhaps preconfigured, directional firing would be consistent with the early appearance of this behavior in humans.

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Science 18 June 2010: Vol. 328. no. 5985, pp. 1576 - 1580

Development of the Spatial Representation System in the Rat

Rosamund F. Langston,1 James A. Ainge,1,2 Jonathan J. Couey,1 Cathrin B. Canto,1 Tale L. Bjerknes,1 Menno P. Witter,1 Edvard I. Moser,1 May-Britt Moser1

1 Kavli Institute for Systems Neuroscience and Centre for the Biology of Memory, Medical Technical Research Center, Norwegian University of Science and Technology, Olav Kyrres gate 9, 7489 Trondheim, Norway.
2 School of Psychology, University of St. Andrews, St. Mary’s Quad, South Street, St. Andrews, Fife KY16 9JP, Scotland.


In the adult brain, space and orientation are represented by an elaborate hippocampal-parahippocampal circuit consisting of head-direction cells, place cells, and grid cells. We report that a rudimentary map of space is already present when 21/2-week-old rat pups explore an open environment outside the nest for the first time. Head-direction cells in the pre- and parasubiculum have adultlike properties from the beginning. Place and grid cells are also present but evolve more gradually. Grid cells show the slowest development. The gradual refinement of the spatial representation is accompanied by an increase in network synchrony among entorhinal stellate cells. The presence of adultlike directional signals at the onset of navigation raises the possibility that such signals are instrumental in setting up networks for place and grid representation.

The hippocampus and entorhinal cortex are key components of the brain’s network for representing an animal’s position in external space. In the hippocampus, place cells fire selectively when the animal visits a specific part of the environment. Cortical inputs to place cells are likely to originate from entorhinal grid cells one or two synapses upstream. These cells have multiple discrete firing locations that, for each cell, define a periodic hexagonal array across the full extent of any space available to the animal. Together with head-direction cells and border cells located in the same brain region, grid cells are thought to provide the key elements of a path integration–based spatial map in which the animal’s position can be updated dynamically in accordance with its own movements.

Our study has two main findings. First, head-direction cells, place cells, and grid cells were detected when rat pups navigated spaces outside the nest for the first times in their lives. The three cell types may interact from the outset, with rudimentary grid cells providing sufficiently patterned input to the hippocampus to generate place-specific firing in this region. Second, directional and positional components of the representation were found to mature at different rates. Head-direction cells in pre- and parasubiculum showed adultlike properties when the pups left the nest for the first time, often only hours after the eyelids had unsealed, whereas grid and place cells continued to evolve, with many grid cells not reaching adultlike levels of spatial periodicity until about 4 weeks of age. Because connections from pre- and parasubiculum to medial entorhinal cortex (MEC) were already functional at P16, the early representation of direction in pre- and parasubiculum may be instrumental in the subsequent development of adultlike grid and place maps in entorhinal cortex and hippocampus.

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Return to — Orientation

Further discussion -- Covington Theory of Consciousness

Figure 1

Exploring a new environment. In rat pups, a given place cell in the hippocampus fires whenever the animal traverses a particular location within the environment; a given direction cell fires whenever the animal's head faces in a certain direction relative to its environment; and a given grid cell fires at the vertices of a regular, repeating grid that covers the environment. The direction and place cells are present when pups make their first such exploration; the time of grid cell appearance is disputed.