Specialized contributions of mid-tier stages of dorsal and ventral pathways to stereoscopic processing in macaque
Abstract
The division of labor between the dorsal and ventral visual pathways has been well studied, but not often with direct comparison at the single-neuron resolution with matched stimuli. Here we directly compared how single neurons in MT and V4, mid-tier areas of the two pathways, process binocular disparity, a powerful cue for 3D perception and actions. We found that MT neurons transmitted disparity signals more quickly and robustly, whereas V4 or its upstream neurons transformed the signals into sophisticated representations more prominently. Therefore, signaling speed and robustness were traded for transformation between the dorsal and ventral pathways. The key factor in this tradeoff was disparity-tuning shape: V4 neurons had more even-symmetric tuning than MT neurons. Moreover, the tuning symmetry predicted the degree of signal transformation across neurons similarly within each area, implying a general role of tuning symmetry in the stereoscopic processing by the two pathways.
Data availability
Source data files have been provided for all data figures.
Article and author information
Author details
Funding
Ministry of Education, Culture, Sports, Science and Technology (2324007)
- Ichiro Fujita
Ministry of Education, Culture, Sports, Science and Technology (15H01437)
- Ichiro Fujita
Ministry of Education, Culture, Sports, Science and Technology (17H01381)
- Ichiro Fujita
Ministry of Education, Culture, Sports, Science and Technology (18H05007)
- Ichiro Fujita
Ministry of Internal Affairs and Communications
- Ichiro Fujita
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: All experimental procedures in this study were approved by the Animal Experiment Committee (Permit Numbers: FBS-12-016, FBS-13-003-1) of Osaka University, and conformed to the Guide for the Care and Use of Laboratory Animals issued by the National Institutes of Health, USA.
Copyright
© 2021, Yoshioka 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
-
- 1,264
- views
-
- 105
- downloads
-
- 6
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
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)
Further reading
-
- Developmental Biology
- Neuroscience
In a developing nervous system, axonal arbors often undergo complex rearrangements before neural circuits attain their final innervation topology. In the lateral line sensory system of the zebrafish, developing sensory axons reorganize their terminal arborization patterns to establish precise neural microcircuits around the mechanosensory hair cells. However, a quantitative understanding of the changes in the sensory arbor morphology and the regulators behind the microcircuit assembly remain enigmatic. Here, we report that Semaphorin7A (Sema7A) acts as an important mediator of these processes. Utilizing a semi-automated three-dimensional neurite tracing methodology and computational techniques, we have identified and quantitatively analyzed distinct topological features that shape the network in wild-type and Sema7A loss-of-function mutants. In contrast to those of wild-type animals, the sensory axons in Sema7A mutants display aberrant arborizations with disorganized network topology and diminished contacts to hair cells. Moreover, ectopic expression of a secreted form of Sema7A by non-hair cells induces chemotropic guidance of sensory axons. Our findings propose that Sema7A likely functions both as a juxtracrine and as a secreted cue to pattern neural circuitry during sensory organ development.
-
- Neuroscience
Pavlovian fear conditioning research suggests that the interaction between the dorsal periaqueductal gray (dPAG) and basolateral amygdala (BLA) acts as a prediction error mechanism in the formation of associative fear memories. However, their roles in responding to naturalistic predatory threats, characterized by less explicit cues and the absence of reiterative trial-and-error learning events, remain unexplored. In this study, we conducted single-unit recordings in rats during an ‘approach food-avoid predator’ task, focusing on the responsiveness of dPAG and BLA neurons to a rapidly approaching robot predator. Optogenetic stimulation of the dPAG triggered fleeing behaviors and increased BLA activity in naive rats. Notably, BLA neurons activated by dPAG stimulation displayed immediate responses to the robot, demonstrating heightened synchronous activity compared to BLA neurons that did not respond to dPAG stimulation. Additionally, the use of anterograde and retrograde tracer injections into the dPAG and BLA, respectively, coupled with c-Fos activation in response to predatory threats, indicates that the midline thalamus may play an intermediary role in innate antipredatory-defensive functioning.