Functionally defined white matter of the macaque monkey brain reveals a dorso-ventral attention network
Abstract
Classical studies of attention have identified areas of parietal and frontal cortex as sources of attentional control. Recently, a ventral region in the macaque temporal cortex, the posterior infero-temporal dorsal area PITd, has been suggested as a third attentional control area. This raises the question of whether and how spatially distant areas coordinate a joint focus of attention. Here we tested the hypothesis that parieto-frontal attention areas and PITd are directly interconnected. By combining functional MRI with ex-vivo high-resolution diffusion MRI, we found that PITd and dorsal attention areas are all directly connected through three specific fascicles. These results ascribe a new function, the communication of attention signals, to two known fiber-bundles, highlight the importance of vertical interactions across the two visual streams, and imply that the control of endogenous attention, hitherto thought to reside in macaque dorsal cortical areas, is exerted by a dorso-ventral network.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files. Source data for Figures 2, 3, 4, 5, have been made available via the Open Science Framework (https://osf.io/8ks5t/).
-
Functionally defined white matter of the macaque monkey brain reveals a dorso-ventral attention network - DataOpen Science Framework, 10.17605/OSF.IO/8KS5T.
Article and author information
Author details
Funding
Leon Levy Foundation (https://leonlevyfoundation.org/leon-levy-fellowship-neuroscience)
- Ilaria Sani
National Science Foundation (BCS-1734853)
- Franco Pestilli
New York Stem Cell Foundation (https://nyscf.org)
- Winrich A Freiwald
National Science Foundation (BCS-1057006)
- Winrich A Freiwald
National Institutes of Health (NIMH ULTTR001108)
- Franco Pestilli
Indiana Clinical and Translational Sciences Institute (Passthrough)
- Franco Pestilli
Microsoft Research (Azure Credits Award)
- Franco Pestilli
Indiana University (Areas of Emergent Research initiative Learning: Brains-Machines-Children)
- Franco Pestilli
National Institutes of Health (1U54MH091657)
- Franco Pestilli
National Science Foundation (IIS-1636893)
- Franco Pestilli
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: Our Protocols protocol has been approved by The Rockefeller University, Institutional Animal Care and Use Committee. In vivo imaging procedures were performed at the Center for Advanced Imaging of Bremen University. They conformed to the National Institutes of Health Guide for Use and Care of Laboratory Animals, regulations for the welfare of experimental animals issued by the federal government of Germany,and stipulations of local Bremen authorities
Copyright
© 2019, Sani 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
-
- 3,361
- views
-
- 506
- downloads
-
- 46
- 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
-
- Neuroscience
Learning alters cortical representations and improves perception. Apical tuft dendrites in cortical layer 1, which are unique in their connectivity and biophysical properties, may be a key site of learning-induced plasticity. We used both two-photon and SCAPE microscopy to longitudinally track tuft-wide calcium spikes in apical dendrites of layer 5 pyramidal neurons in barrel cortex as mice learned a tactile behavior. Mice were trained to discriminate two orthogonal directions of whisker stimulation. Reinforcement learning, but not repeated stimulus exposure, enhanced tuft selectivity for both directions equally, even though only one was associated with reward. Selective tufts emerged from initially unresponsive or low-selectivity populations. Animal movement and choice did not account for changes in stimulus selectivity. Enhanced selectivity persisted even after rewards were removed and animals ceased performing the task. We conclude that learning produces long-lasting realignment of apical dendrite tuft responses to behaviorally relevant dimensions of a task.
-
- Neuroscience
Multiplexed error-robust fluorescence in situ hybridization (MERFISH) allows genome-scale imaging of RNAs in individual cells in intact tissues. To date, MERFISH has been applied to image thin-tissue samples of ~10 µm thickness. Here, we present a thick-tissue three-dimensional (3D) MERFISH imaging method, which uses confocal microscopy for optical sectioning, deep learning for increasing imaging speed and quality, as well as sample preparation and imaging protocol optimized for thick samples. We demonstrated 3D MERFISH on mouse brain tissue sections of up to 200 µm thickness with high detection efficiency and accuracy. We anticipate that 3D thick-tissue MERFISH imaging will broaden the scope of questions that can be addressed by spatial genomics.