Navigating space in the mammalian brain

doi:10.1126/science.abi9663

GSTDTAP > 气候变化

DOI	10.1126/science.abi9663
	Navigating space in the mammalian brain
	Emma R. Wood; Paul A. Dudchenko
	2021-05-28
发表期刊	Science
出版年	2021
英文摘要	How does the brain represent the world and allow spatial navigation? One mechanism is hippocampal place cells—neurons that fire according to where an animal is in its environment. Different place cells fire according to different locations, and together they are thought to provide a cognitive map that supports spatial navigation and memory ([ 1 ][1]). Place cells have been described in a range of mammalian species, including mice, bats, marmosets, and humans. However, most studies have used rats in small enclosures or mazes. Thus, it is unknown how such representations might underpin larger-scale, real-world navigation. On page 933 of this issue, Eliav et al. ([ 2 ][2]) show that in bats flying in a large (200-m-long) enclosure, most place cells fire in several different locations and with varying spatial scales. Such multiscale representations are likely the most efficient way for a finite number of neurons to encode large distances. Neurophysiological recordings in rats exploring relatively small “open-field” environments (∼1 m2) or running along short tracks 1 to 2 m long have revealed that a given place cell in the hippocampus typically fires when the rat is in a single area within the apparatus (called its place field) ([ 1 ][1], [ 3 ][3], [ 4 ][4]). In the few experiments that have investigated bigger open-field environments and longer tracks, place fields are typically slightly enlarged compared with those in smaller environments ([ 4 ][4]–[ 6 ][5]), and individual place cells in CA1 (the main output region of the hippocampus) fire in multiple, irregularly spaced locations ([ 5 ][6], [ 6 ][5]), with more place fields per cell in tracks of increasing length ([ 6 ][5]). Within a given environment, the different place fields of each hippocampal neuron are of a fairly uniform size, but there is an anatomical gradient, with the most dorsal hippocampal place cells having the smallest fields and ventral hippocampal cells having the largest fields ([ 3 ][3], [ 7 ][7]). Together, these studies suggest that the hippocampus provides an ensemble place code, whereby different combinations of neurons are active in any given location, and that coding of different spatial scales is provided by different neurons across the dorsal-ventral hippocampal axis. But how does the mammalian brain represent much larger spaces, on the spatial scale that animals would need to navigate in their natural environment? Eliav et al. wirelessly recorded from dorsal CA1 place cells in bats as they flew along a 200-m-long tunnel between two feeding stations. They found not only that place cells expressed multiple, irregularly spaced place fields in this very large environment but also that the size of the different place fields expressed by a given neuron varied widely: The mean ratio of the largest:smallest field was 4.4:1, but this was as high as 20:1 in some cells (see the figure). By contrast, and consistent with observations in rats, in a shorter 6-m-long tunnel, place cells expressed only one or two fields, the average field size was smaller than in the 200-mlong tunnel, and fields of the same cell were of a similar size (mean ratio <2:1). ![Figure][8] Navigating large, complex spaces Eliav et al. found that bats exhibit multiscale place cell coding. Individual place cells in the hippocampus fire according to a range of spatial scales (place fields of a single place cell indicated by circles), allowing optimal processing of a large environment with a finite number of cells. GRAPHIC: N. DESAI/ SCIENCE These findings of multiscale coding by individual place cells may help answer a puzzling question: How can a finite population of place cells encode the large environments in which mammals navigate in the wild, at both large and small spatial scales? The modeling by Eliav et al. shows that the multiscale coding mechanism seen in the bats is a particularly efficient mechanism for coding large environments. It needs fewer neurons for accurate decoding of the current location of the bat than other ensemble coding mechanisms based on individual cells having multiple fields of the same size and other cells having fields of different sizes (as had previously been assumed). It will be important to determine the extent to which multiscale coding by individual neurons is a general property of hippocampal coding across species and across different types and scales of environments. A preliminary study of rats following a moving robotic feeder in an 18.6-m2 open-field environment reported that cells in dorsal CA1 exhibited the same type of multiscale coding as found in the tunnel-flying bats ([ 8 ][9]). This indicates that this type of firing may be a general principle of hippocampal coding of large-scale space across mammalian species. Moreover, perhaps in large, continuous spaces, multiscale place cell representation may be the rule. As with many elegant studies, the work of Eliav et al. points to promising new avenues of research. One key question is how multiscale encoding arises. The two main inputs to CA1 (where the multiscale place cells have been described) are the CA3 and the medial entorhinal cortex (MEC). CA3 also contains place cells; indeed, the dorsal-ventral gradient of small-large place fields was described in CA3 neurons in rats ([ 7 ][7]). Conversely, the MEC contains a different type of spatial cell called grid cells. Each grid cell fires in multiple locations arranged in a regular hexagonal grid pattern that repeats across the environment (again with a dorsal-ventral arrangement of grid field size and spacing) ([ 9 ][10], [ 10 ][11]). Grid cells are thought to be important for path integration, where animals use self-motion signals to estimate distances and directions traveled. Eliav et al. suggest a feed-forward model whereby the multiscale fields in CA1 result from convergence of inputs from multiple CA3 place cells with different spatial scales onto each CA1 place cell. Predictions of this model that still need to be tested are that CA3 neurons should not show multiple fields in large environments and that either grid cells should not show multiple fields or grid cell inputs do not contribute to the firing of CA1 place fields in large environments. A second question is whether there is a continuum of multiscale coding across environments of all sizes or whether (as suggested by Eliav et al. ) multiscale coding occurs only in sufficiently large environments. And if the latter, what behavioral, perceptual, and neural mechanisms trigger the transition from small-scale to large-scale encoding of space? The study of Eliav et al. provides a marker for the need to examine spatial coding in ethologically relevant environments. The multiscale place cell coding mechanism that they demonstrate may allow both fine-scale spatial localization and localization on a more extended scale, which would be required for navigating accurately between very distant locations hundreds of meters or kilometers apart. 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领域	气候变化 ; 资源环境
URL	查看原文
引用统计	被引频次：1[WOS] [WOS记录] [WOS相关记录]
文献类型	期刊论文
条目标识符	http://119.78.100.173/C666/handle/2XK7JSWQ/328854
专题	气候变化资源环境科学
推荐引用方式 GB/T 7714	Emma R. Wood,Paul A. Dudchenko. Navigating space in the mammalian brain[J]. Science,2021.
APA	Emma R. Wood,&Paul A. Dudchenko.(2021).Navigating space in the mammalian brain.Science.
MLA	Emma R. Wood,et al."Navigating space in the mammalian brain".Science (2021).