Sensory cortex is optimised for prediction of future input
- University of Oxford, United Kingdom
- City University of Hong Kong, Hong Kong
Abstract
Neurons in sensory cortex are tuned to diverse features in natural scenes. But what determines which features neurons become selective to? Here we explore the idea that neuronal selectivity is optimised to represent features in the recent sensory past that best predict immediate future inputs. We tested this hypothesis using simple feedforward neural networks, which were trained to predict the next few video or audio frames in clips of natural scenes. The networks developed receptive fields that closely matched those of real cortical neurons in different mammalian species, including the oriented spatial tuning of primary visual cortex, the frequency selectivity of primary auditory cortex and, most notably, their temporal tuning properties. Furthermore, the better a network predicted future inputs the more closely its receptive fields resembled those in the brain. This suggests that sensory processing is optimised to extract those features with the most capacity to predict future input.
Data availability
All custom code used in this study was implemented in MATLAB and Python. We have uploaded the code to a public Github repository. The raw auditory experimental data is available at https://osf.io/ayw2p/. The movies and sounds used for training the models are all publicly available at the websites detailed in the Methods.
Article and author information
Author details
Funding
Clarendon Fund
- Yosef Singer
- Yayoi Teramoto
University Of Oxford
- Nicol S Harper
Action on Hearing Loss (PA07)
- Nicol S Harper
Biotechnology and Biological Sciences Research Council (BB/H008608/1)
- Nicol S Harper
Wellcome (WT10525/Z/14/Z)
- Yayoi Teramoto
Wellcome (WT076508AIA)
- Ben DB Willmore
Wellcome (WT108369/Z/2015/Z)
- Ben DB Willmore
Wellcome (WT076508AIA)
- Andrew J King
Wellcome (WT108369/Z/2015/Z)
- Andrew J King
Wellcome (WT082692)
- Nicol S Harper
Wellcome (WT076508AIA)
- Nicol S Harper
Wellcome (WT108369/Z/2015/Z)
- Nicol S Harper
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: Auditory RFs of neurons were recorded in the primary auditory cortex (A1) and anterior auditory field (AAF) of 5 pigmented ferrets of both sexes (all > 6 months of age) and used as a basis for comparison with the RFs of model units trained on auditory stimuli. These recordings were performed under license from the UK Home Office and were approved by the University of Oxford Committee on Animal Care and Ethical Review. Full details of the recording methods are described in earlier studies [45,90]. Briefly, we induced general anaesthesia with a single intramuscular dose of medetomidine (0.022 mg · kg−1 · h−1) and ketamine (5 mg · kg−1 · h−1), which was then maintained with a continuous intravenous infusion of medetomidine and ketamine in saline. Oxygen was supplemented with a ventilator, and we monitored vital signs (body temperature, end-tidal CO2, and the electrocardiogram) throughout the experiment. The temporal muscles were retracted, a head holder was secured to the skull surface, and a craniotomy and a durotomy were made over the auditory cortex. Extracellular recordings were made using silicon probe electrodes (Neuronexus Technologies) and acoustic stimuli were presented via Panasonic RPHV27 earphones, which were coupled to otoscope specula that were inserted into each ear canal, and driven by Tucker-Davis Technologies System III hardware (48 kHz sample rate).
Copyright
© 2018, Singer 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
-
- 7,919
- views
-
- 1,166
- downloads
-
- 58
- 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)
Sensory cortex is optimised for prediction of future input
eLife 7:e31557.
https://doi.org/10.7554/eLife.31557
Further reading
-
- Neuroscience
We used diffusion MRI and x-ray synchrotron imaging on monkey and mice brains to examine the organisation of fibre pathways in white matter across anatomical scales. We compared the structure in the corpus callosum and crossing fibre regions and investigated the differences in cuprizone-induced demyelination in mouse brains versus healthy controls. Our findings revealed common principles of fibre organisation that apply despite the varying patterns observed across species; small axonal fasciculi and major bundles formed laminar structures with varying angles, according to the characteristics of major pathways. Fasciculi exhibited non-straight paths around obstacles like blood vessels, comparable across the samples of varying fibre complexity and demyelination. Quantifications of fibre orientation distributions were consistent across anatomical length scales and modalities, whereas tissue anisotropy had a more complex relationship, both dependent on the field-of-view. Our study emphasises the need to balance field-of-view and voxel size when characterising white matter features across length scales.
-
- Biochemistry and Chemical Biology
- Neuroscience
The buildup of knot-like RNA structures in brain cells may be the key to understanding how uncontrolled protein aggregation drives Alzheimer’s disease.
