Mice and primates use distinct strategies for visual segmentation
- California Institute of Technology, United States
- University of Geneva, Switzerland
- University of California, Berkeley, United States
Abstract
The rodent visual system has attracted great interest in recent years due to its experimental tractability, but the fundamental mechanisms used by the mouse to represent the visual world remain unclear. In the primate, researchers have argued from both behavioral and neural evidence that a key step in visual representation is 'figure-ground segmentation', the delineation of figures as distinct from backgrounds (Nakayama, He, and Shimojo 1995; Lamme 1995; Poort et al. 2012; Qiu and Heydt 2005). To determine if mice also show behavioral and neural signatures of figure-ground segmentation, we trained mice on a figure-ground segmentation task where figures were defined by gratings and naturalistic textures moving counterphase to the background. Unlike primates, mice were severely limited in their ability to segment figure from ground using the opponent motion cue, with segmentation behavior strongly dependent on the specific carrier pattern. Remarkably, when mice were forced to localize naturalistic patterns defined by opponent motion, they adopted a strategy of brute force memorization of texture patterns. In contrast, primates, including humans, macaques, and mouse lemurs, could readily segment figures independent of carrier pattern using the opponent motion cue. Consistent with mouse behavior, neural responses to the same stimuli recorded in mouse visual areas V1, RL, and LM also did not support texture-invariant segmentation of figures using opponent motion. Modeling revealed that the texture dependence of both the mouse's behavior and neural responses could be explained by a feedforward neural network lacking explicit segmentation capabilities. These findings reveal a fundamental limitation in the ability of mice to segment visual objects compared to primates.
Data availability
Source data has been provided to replicate all neural and behavioral figures (2,3,4,5,6,7). These data have been uploaded to dryad: https://doi.org/10.5061/dryad.ngf1vhhvp.Sufficient modeling details have been provided in methods section to replicate relevant parts of figure 8.
-
Data from: Mice and primates use distinct strategies for visual segmentationDryad Digital Repository, doi:10.5061/dryad.ngf1vhhvp.
Article and author information
Author details
Funding
NIH , Howard Hughes Medical Institute
- Doris Y Tsao
Arnold O. Beckman postdoctoral fellowship, Burroughs Wellcome PDEP Award
- Francisco J Luongo
Swiss National Science Foundation
- Daniel Huber
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: The following animals were used in this study: adult mice 2-12 months old, both male and female; adult treeshrews 7-18 months old, both male and female; adult mouse lemurs 2-3.5 yrs, both male and female; and adult macaques 3 and 7 yrs old, male. All procedures on mice, macaques, and tree shrews were conducted in accordance with the ethical guidelines of the National Institutes of Health and were approved by the Institutional Animal Care and Use Committee at the California Institute of Technology.Mouse lemur experiments were in accordance with European animal welfare regulations and were reviewed by the local ethics committee ('Comite d'éthique en expérimentation animale No. 68') in Brunoy, France, by the ethics committee of the University of Geneva, Switzerland and authorized by the French 'Ministère de l'education nationale de l'enseignement supérieur et de la recherche."
Copyright
© 2023, Luongo et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 2,904
- views
-
- 340
- downloads
-
- 10
- 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)
Mice and primates use distinct strategies for visual segmentation
eLife 12:e74394.
https://doi.org/10.7554/eLife.74394
Further reading
-
- Cancer Biology
- Evolutionary Biology
In growing cell populations such as tumours, mutations can serve as markers that allow tracking the past evolution from current samples. The genomic analyses of bulk samples and samples from multiple regions have shed light on the evolutionary forces acting on tumours. However, little is known empirically on the spatio-temporal dynamics of tumour evolution. Here, we leverage published data from resected hepatocellular carcinomas, each with several hundred samples taken in two and three dimensions. Using spatial metrics of evolution, we find that tumour cells grow predominantly uniformly within the tumour volume instead of at the surface. We determine how mutations and cells are dispersed throughout the tumour and how cell death contributes to the overall tumour growth. Our methods shed light on the early evolution of tumours in vivo and can be applied to high-resolution data in the emerging field of spatial biology.
-
- Evolutionary Biology
Spatial patterns in genetic diversity are shaped by individuals dispersing from their parents and larger-scale population movements. It has long been appreciated that these patterns of movement shape the underlying genealogies along the genome leading to geographic patterns of isolation by distance in contemporary population genetic data. However, extracting the enormous amount of information contained in genealogies along recombining sequences has, until recently, not been computationally feasible. Here we capitalize on important recent advances in genome-wide gene-genealogy reconstruction and develop methods to use thousands of trees to estimate per-generation dispersal rates and to locate the genetic ancestors of a sample back through time. We take a likelihood approach in continuous space using a simple approximate model (branching Brownian motion) as our prior distribution of spatial genealogies. After testing our method with simulations we apply it to Arabidopsis thaliana. We estimate a dispersal rate of roughly 60km2 per generation, slightly higher across latitude than across longitude, potentially reflecting a northward post-glacial expansion. Locating ancestors allows us to visualize major geographic movements, alternative geographic histories, and admixture. Our method highlights the huge amount of information about past dispersal events and population movements contained in genome-wide genealogies.
