Spatial Navigation: A question of scale

An fMRI experiment reveals distinct brain regions that respond in a graded manner as humans process distance information across increasing spatial scales.
  1. Muireann Irish  Is a corresponding author
  2. Siddharth Ramanan
  1. University of Sydney, Australia
  2. Macquarie University, Australia

Just like our ancestors before us, humans must be able to navigate within both familiar and new environments, whether this involves driving to work or finding our way around a new city. Successful spatial navigation depends on many cognitive processes including memory, attention, and our perception of direction and distance (Epstein et al., 2017). A key issue, however, is that spatial environments vary considerably in terms of their size and complexity. To date most research on spatial navigation has focused on small spatial scales, such as navigating within a room or a building (Wolbers and Wiener, 2014). But it remains unclear how accurately we can estimate distances between locations on a larger scale, such as whether the Taj Mahal is closer to the Pyramids of Giza or the Great Wall of China, and how these different spatial scales are represented in the brain.

Now, in eLife, Michael Peer, Yorai Ron, Rotem Monsa and Shahar Arzy – who are based at the Hebrew University of Jerusalem, the Hadassah Medical Center and the University of Pennsylvania – report a simple but elegant experiment that teases apart which brain regions are recruited when we process information about environments that are on different spatial scales (Peer et al., 2019). Peer et al. asked internationally-travelled adults to provide the names of two locations they were personally familiar with across six spatial ‘scales’. These scales varied from small, spatially-confined areas (e.g. rooms and buildings) through medium-sized regions (e.g. local neighborhoods and cities) to expansive geographical locations (e.g. countries and continents; Figure 1A). The experiment was then personalized by asking each participant to provide the names of eight items that were personally familiar to them within each location.

How different spatial environments are represented in the human brain.

(A) In order to navigate successfully humans must be able to judge distances between objects on both small (e.g. rooms and buildings) and large (e.g. cities and countries) scales. (B) Peer et al. showed that estimating distance across different spatial scales engages three main clusters of brain regions that are organized along a gradient (represented by the white dashed lines in each hemisphere). Within each cluster, spatial environments that are smaller and more constrained (red and orange) are represented in posterior portions, whilst larger, less-constrained environments (blue and purple) are represented in more anterior portions of the clusters. The middle surface of the brain (where the right and left hemispheres meet) is shown in the upper panels; the outer surfaces of the two hemispheres are shown below.

Image credit: Adapted from Peer et al. (2019).

A few days later, participants underwent a functional magnetic resonance imaging experiment to determine which areas of the brain are selectively involved during spatial processing. This technique enables researchers to measure increases in blood flow and oxygen delivery to parts of the brain, and determine which regions are more ‘active’ when engaging in a cognitive task. During the experiment, participants were asked to judge distances between a ‘target’ item from their personal list (e.g. a table in their bedroom) and two other items from the same location (e.g. a chair or a bed in their bedroom). This allowed Peer et al. to investigate which brain regions respond to small, medium, and large spatial scales, and which regions are insensitive to scale but respond to other location or proximity information.

The experiment identified three main clusters of brain regions that are important for processing different spatial scales. What was unique about all three clusters was that activity within them shifted in a ‘graded’ manner depending on whether participants were processing spatial information on a local or more global scale. For example, when participants judged distances on a small scale in local environments, this engaged the posterior portions of all three clusters. On the other hand, when participants judged distances on a larger scale, the pattern of activity shifted towards the anterior portions of the clusters (Figure 1B).

These findings align remarkably well with previous work showing that the human hippocampus – a region of the brain involved in spatial navigation (Burgess et al., 2002) – represents object position and spatial information, such as direction and distance between objects, as a graded pattern of activity (Evensmoen et al., 2015; Evensmoen et al., 2013). The latest study, however, extends our understanding by highlighting how graded patterns of activity move from posterior to anterior regions of the spatial processing network outside of the hippocampus, depending on the spatial scale being processed (Figure 1).

The work presented here provides new insights into how humans navigate within different environments. From a clinical perspective, appreciating how humans dynamically zoom in or out of different spatial scales could help refine how various neurological conditions are diagnosed. This is most relevant for neurodegenerative disorders, such as Alzheimer’s disease, in which disorientation and a distorted sense of direction are often early symptoms (Coughlan et al., 2018; Tu et al., 2015). Whether the altered sense of direction and difficulties in judging proximity that are associated with Alzheimer’s disease are due to changes in the way that regions of the brain represent spatial scale is an important question for future studies to address.

References

Article and author information

Author details

  1. Muireann Irish

    Muireann Irish is in the Brain and Mind Centre and School of Psychology, University of Sydney, Sydney, Australia, and the ARC Centre of Excellence in Cognition and its Disorders, Macquarie University, North Ryde, Australia

    For correspondence
    muireann.irish@sydney.edu.au
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4950-8169
  2. Siddharth Ramanan

    Siddharth Ramanan is in the Brain and Mind Centre and School of Psychology, University of Sydney, Sydney, Australia, and the ARC Centre of Excellence in Cognition and its Disorders, Macquarie University, North Ryde, Australia

    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8591-042X

Publication history

  1. Version of Record published:

Copyright

© 2019, Irish and Ramanan

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,897
    views
  • 120
    downloads
  • 1
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Muireann Irish
  2. Siddharth Ramanan
(2019)
Spatial Navigation: A question of scale
eLife 8:e50890.
https://doi.org/10.7554/eLife.50890
  1. Further reading

Further reading

    1. Cell Biology
    2. Neuroscience
    Luis Sánchez-Guardado, Peyman Callejas Razavi ... Carlos Lois
    Research Article

    The assembly and maintenance of neural circuits is crucial for proper brain function. Although the assembly of brain circuits has been extensively studied, much less is understood about the mechanisms controlling their maintenance as animals mature. In the olfactory system, the axons of olfactory sensory neurons (OSNs) expressing the same odor receptor converge into discrete synaptic structures of the olfactory bulb (OB) called glomeruli, forming a stereotypic odor map. The OB projection neurons, called mitral and tufted cells (M/Ts), have a single dendrite that branches into a single glomerulus, where they make synapses with OSNs. We used a genetic method to progressively eliminate the vast majority of M/T cells in early postnatal mice, and observed that the assembly of the OB bulb circuits proceeded normally. However, as the animals became adults the apical dendrite of remaining M/Ts grew multiple branches that innervated several glomeruli, and OSNs expressing single odor receptors projected their axons into multiple glomeruli, disrupting the olfactory sensory map. Moreover, ablating the M/Ts in adult animals also resulted in similar structural changes in the projections of remaining M/Ts and axons from OSNs. Interestingly, the ability of these mice to detect odors was relatively preserved despite only having 1–5% of projection neurons transmitting odorant information to the brain, and having highly disrupted circuits in the OB. These results indicate that a reduced number of projection neurons does not affect the normal assembly of the olfactory circuit, but induces structural instability of the olfactory circuitry of adult animals.

    1. Neuroscience
    GVS Devakinandan, Mark Terasaki, Adish Dani
    Research Article

    Specialized chemosensory signals elicit innate social behaviors in individuals of several vertebrate species, a process that is mediated via the accessory olfactory system (AOS). The AOS comprising the peripheral sensory vomeronasal organ has evolved elaborate molecular and cellular mechanisms to detect chemo signals. To gain insight into the cell types, developmental gene expression patterns, and functional differences amongst neurons, we performed single-cell transcriptomics of the mouse vomeronasal sensory epithelium. Our analysis reveals diverse cell types with gene expression patterns specific to each, which we made available as a searchable web resource accessed from https://www.scvnoexplorer.com. Pseudo-time developmental analysis indicates that neurons originating from common progenitors diverge in their gene expression during maturation with transient and persistent transcription factor expression at critical branch points. Comparative analysis across two of the major neuronal subtypes that express divergent GPCR families and the G-protein subunits Gnai2 or Gnao1, reveals significantly higher expression of endoplasmic reticulum (ER) associated genes within Gnao1 neurons. In addition, differences in ER content and prevalence of cubic membrane ER ultrastructure revealed by electron microscopy, indicate fundamental differences in ER function.