Constructing the hierarchy of predictive auditory sequences in the marmoset brain
- Chinese Academy of Sciences, China
- Center for Brain Science, RIKEN, Japan
Abstract
Our brains constantly generate predictions of sensory input that are compared with actual inputs, propagate the prediction-errors through a hierarchy of brain regions, and subsequently update the internal predictions of the world. However, the essential feature of predictive coding, the notion of hierarchical depth and its neural mechanisms, remains largely unexplored. Here, we investigated the hierarchical depth of predictive auditory processing by combining functional magnetic resonance imaging (fMRI) and high-density whole-brain electrocorticography (ECoG) in marmoset monkeys during an auditory local-global paradigm in which the temporal regularities of the stimuli were designed at two hierarchical levels. The prediction-errors and prediction updates were examined as neural responses to auditory mismatches and omissions. Using fMRI, we identified a hierarchical gradient along the auditory pathway: midbrain and sensory regions represented local, shorter-time-scale predictive processing followed by associative auditory regions, whereas anterior temporal and prefrontal areas represented global, longer-time-scale sequence processing. The complementary ECoG recordings confirmed the activations at cortical surface areas and further differentiated the signals of prediction-error and update, which were transmitted via putative bottom-up g and top-down b oscillations, respectively. Furthermore, omission responses caused by absence of input, reflecting solely the two levels of prediction signals that are unique to the hierarchical predictive coding framework, demonstrated the hierarchical top-down process of predictions in the auditory, temporal, and prefrontal areas. Thus, our findings support the hierarchical predictive coding framework, and outline how neural networks and spatiotemporal dynamics are used to represent and arrange a hierarchical structure of auditory sequences in the marmoset brain.
Data availability
The fMRI and ECoG data that support the findings of this study are publicly available in Dryad: Jiang, Yuwei (2021), Constructing the hierarchy of predictive auditory sequences in the marmoset brain, Dryad, Dataset, https://doi.org/10.5061/dryad.j3tx95xfp.
-
Data from: Constructing the hierarchy of predictive auditory sequences in the marmoset brainDryad Digital Repository, doi:10.5061/dryad.j3tx95xfp.
Article and author information
Author details
Funding
National Science and Technology Innovation 2030 Major Program (2021ZD0204102)
- Liping Wang
Youth Innovation Promotion Association Chinese Academy of Sciences
- Yuwei Jiang
Brain/MINDS from the Japan Agency for Medical Research and Development (JP20dm0207069)
- Misako Komatsu
JSPS KAKENHI (JP19H04993)
- Misako Komatsu
Strategic Priority Research Program (XDB32070201)
- Liping Wang
Strategic Priority Research Program (XDB32030100)
- Liping Wang
Strategic Priority Research Program (XDBS01030100)
- Zhifeng Liang
Pioneer Hundreds of Talents Program from the Chinese Academy of Sciences
- Zhifeng Liang
- Liping Wang
Shanghai Municipal Science and Technology Major Project (2018SHZDZX05)
- Liping Wang
Shanghai Municipal Science and Technology Major Project (2018SHZDZX05)
- Zhifeng Liang
National Natural Science Foundation of China (81801354)
- Zhifeng Liang
National Natural Science Foundation of China (31900797)
- Yuwei Jiang
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 protocol of the fMRI study was approved by the Ethical Committee of the Institute of Neuroscience, Chinese Academy of Sciences (no. ION-20180522). All procedures of the ECoG study were conducted in accordance with a protocol approved by the RIKEN Ethical Committee [no. W2020-2-008(2)].
Copyright
© 2022, Jiang 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
-
- 2,354
- views
-
- 494
- downloads
-
- 31
- 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)
Constructing the hierarchy of predictive auditory sequences in the marmoset brain
eLife 11:e74653.
https://doi.org/10.7554/eLife.74653
Further reading
-
- Neuroscience
As the global population ages, the prevalence of neurodegenerative disorders is fast increasing. This neurodegeneration as well as other central nervous system (CNS) injuries cause permanent disabilities. Thus, generation of new neurons is the rosetta stone in contemporary neuroscience. Glial cells support CNS homeostasis through evolutionary conserved mechanisms. Upon damage, glial cells activate an immune and inflammatory response to clear the injury site from debris and proliferate to restore cell number. This glial regenerative response (GRR) is mediated by the neuropil-associated glia (NG) in Drosophila, equivalent to vertebrate astrocytes, oligodendrocytes (OL), and oligodendrocyte progenitor cells (OPCs). Here, we examine the contribution of NG lineages and the GRR in response to injury. The results indicate that NG exchanges identities between ensheathing glia (EG) and astrocyte-like glia (ALG). Additionally, we found that NG cells undergo transdifferentiation to yield neurons. Moreover, this transdifferentiation increases in injury conditions. Thus, these data demonstrate that glial cells are able to generate new neurons through direct transdifferentiation. The present work makes a fundamental contribution to the CNS regeneration field and describes a new physiological mechanism to generate new neurons.
-
- Neuroscience
Brain states fluctuate between exploratory and consummatory phases of behavior. These state changes affect both internal computation and the organism’s responses to sensory inputs. Understanding neuronal mechanisms supporting exploratory and consummatory states and their switching requires experimental control of behavioral shifts and collecting sufficient amounts of brain data. To achieve this goal, we developed the ThermoMaze, which exploits the animal’s natural warmth-seeking homeostatic behavior. By decreasing the floor temperature and selectively heating unmarked areas, we observed that mice avoided the aversive state by exploring the maze and finding the warm spot. In its design, the ThermoMaze is analogous to the widely used water maze but without the inconvenience of a wet environment and, therefore, allows the collection of physiological data in many trials. We combined the ThermoMaze with electrophysiology recording, and report that spiking activity of hippocampal CA1 neurons during sharp-wave ripple events encode the position of mice. Thus, place-specific firing is not confined to locomotion and associated theta oscillations but persist during waking immobility and sleep at the same location. The ThermoMaze will allow for detailed studies of brain correlates of immobility, preparatory–consummatory transitions, and open new options for studying behavior-mediated temperature homeostasis.
