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.
Reviewing Editor
- Martin Vinck, Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Germany
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."
Version history
- Preprint posted: July 5, 2021 (view preprint)
- Received: October 2, 2021
- Accepted: January 22, 2023
- Accepted Manuscript published: February 15, 2023 (version 1)
- Accepted Manuscript updated: February 22, 2023 (version 2)
- Version of Record published: March 2, 2023 (version 3)
- Version of Record updated: March 6, 2023 (version 4)
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
-
- 2,672
- views
-
- 309
- downloads
-
- 8
- 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
-
- Evolutionary Biology
Extant ecdysozoans (moulting animals) are represented by a great variety of soft-bodied or articulated organisms that may or may not have appendages. However, controversies remain about the vermiform nature (i.e. elongated and tubular) of their ancestral body plan. We describe here Beretella spinosa gen. et sp. nov. a tiny (maximal length 3 mm) ecdysozoan from the lowermost Cambrian, Yanjiahe Formation, South China, characterized by an unusual sack-like appearance, single opening, and spiny ornament. Beretella spinosa gen. et sp. nov has no equivalent among animals, except Saccorhytus coronarius, also from the basal Cambrian. Phylogenetic analyses resolve both fossil species as a sister group (Saccorhytida) to all known Ecdysozoa, thus suggesting that ancestral ecdysozoans may have been non-vermiform animals. Saccorhytids are likely to represent an early off-shot along the stem-line Ecdysozoa. Although it became extinct during the Cambrian, this animal lineage provides precious insight into the early evolution of Ecdysozoa and the nature of the earliest representatives of the group.
-
- Biochemistry and Chemical Biology
- Evolutionary Biology
The emergence of new protein functions is crucial for the evolution of organisms. This process has been extensively researched for soluble enzymes, but it is largely unexplored for membrane transporters, even though the ability to acquire new nutrients from a changing environment requires evolvability of transport functions. Here, we demonstrate the importance of environmental pressure in obtaining a new activity or altering a promiscuous activity in members of the amino acid-polyamine-organocation (APC)-type yeast amino acid transporters family. We identify APC members that have broader substrate spectra than previously described. Using in vivo experimental evolution, we evolve two of these transporter genes, AGP1 and PUT4, toward new substrate specificities. Single mutations on these transporters are found to be sufficient for expanding the substrate range of the proteins, while retaining the capacity to transport all original substrates. Nonetheless, each adaptive mutation comes with a distinct effect on the fitness for each of the original substrates, illustrating a trade-off between the ancestral and evolved functions. Collectively, our findings reveal how substrate-adaptive mutations in membrane transporters contribute to fitness and provide insights into how organisms can use transporter evolution to explore new ecological niches.
