Sensory cortex is optimised for prediction of future input
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.
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Further reading
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- Neuroscience
When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
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- Neuroscience
When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.