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Learning mechanisms for perceptual decisions in biological and artificial neural systems

Lead Research Organisation: University of Cambridge
Department Name: Engineering

Abstract

It is common wisdom that practice makes perfect; that is, training improves our ability to solve difficult tasks and acquire new skills. For example, recognising objects in busy scenes or finding a friend in the crowd-seamless as it may seem- poses significant demands on the brain that is called to 1) detect and select targets from clutter, and (2) discriminate whether similar features belong to the same or different objects. Training and experience improve our ability to make these perceptual judgements accurately and rapidly resulting in successful actions. Yet, the way in which our everyday experiences change the brain is complex and the precise mechanisms that the brain employs to solve new problems based on previous experience remain largely unknown.

Here we propose to build models and artificial systems based on state-of-the-art mathematical algorithms that allow us to simulate the workings of the brain and understand better how it learns. In our first study, we will use an inference method developed in artificial intelligence to infer changes in the brain circuits underlying our ability to recognise objects in cluttered scenes, from high-resolution brain imaging data. This will allow us to identify aspects of the brain circuits (for example, suppressive or exciting connections) that change when we train to improve our perceptual judgments. In our second study, we will construct a model of the brain's visual system that, similarly to artificial neural networks, learns from experience by optimising its internal connections. Unlike artificial networks, our proposed model is inspired by our knowledge of the brain's connections and integrates key biological aspects of brain circuitry. By training this network in various perceptual judgement tasks we will make predictions for the brain mechanisms that underlie the brain's ability to improve its judgements.

We test and validate these models against existing data that we collected using state-of-the-art magnetic resonance imaging to trace how the brain changes its functions with learning at much finer resolution than previously possible. Further, we have exploited advances in MR imaging of metabolites to measure GABA, the primary neurotransmitter that the brain uses for suppressing rather than exciting its neurons. We have previously shown that GABA plays a critical role in learning to improve our perceptual skills.

We will use the developed models to understand the link between changes in the brain's function and neurochemistry due to training. In particular, we ask how: a) changes in the brain's neurochemistry link with changes in brain function, b) learning alters the balance in the brain's chemical signals (excitation vs. inhibition) to boost the brain's flexibility and capacity to perform in everyday tasks. Understanding these key brain processes of plasticity will, in turn, inform the design of better artificial systems. These systems will allow us to make new predictions about how the brain works, advancing our understanding of how the brain supports our ability to learn and adapt to change in our environment across the lifespan. Finally, these brain-inspired artificial systems may improve in their learning and advance digital technologies (e.g. brain-computer interface solutions) for patients with neurological disorders that are impaired in their ability to interact with the environment.

Technical Summary

Despite the fundamental role of learning in guiding our decisions, we know surprisingly little about how the brain learns to improve our judgments. Combining recent advances in computational modelling, machine learning, and brain imaging provides a unique opportunity to interrogate the computational principles and fine-scale circuit mechanisms that underlie learning for perceptual decisions.
Here, we propose an AI-inspired computational framework that integrates mechanistic circuit modelling and ultra high-field brain imaging to a) interrogate the adaptive computations and mechanisms that boost skills at the core of visual recognition (i.e. detect targets in clutter; discriminate similar objects), b) compare these mechanisms in biological and artificial systems.
We will use two complimentary model-based approaches to gain insight into the circuit mechanisms and computational principles that underlie learning-induced changes in networks of excitation and inhibition. First, we will adopt a data-driven mechanistic modelling approach; that is, using modern inference methods from machine learning, we will fit a mechanistic model of cortical circuits that we have previously developed to existing brain imaging data (high-resolution fMRI across cortical layers, MR spectroscopy measurements of neurotransmitters). Second, we will adopt a normative approach guided by principles of optimal learning. We will train a deep network model of visual cortex that respects biological constraints on excitatory and inhibitory connectivity. We will test the hypothesis that training optimises perceptual decisions by altering the balance of cortical excitation and inhibition in line with task-specific computations to support adaptive behaviour.
Our cross-disciplinary approach will a) advance our understanding of adaptive brain computations across scales, linking local circuits to whole-brain networks, b) inform the development of next-generation biologically-inspired artificial systems.
 
Description Our visual perceptual acuities can be improved by practice. Using neuroimaging, the co-PI Zoe Kourtzi and her team had previously found that such improvements lead to (a) specific changes in the brain's inhibitory and excitatory connectivity, and (b) increase in the information content of neural activity patterns in the visual cortex, but only in its superficial layers. In this project, we aimed to shed light on the mechanisms and computational principles underlying these findings. Here is a summary of our results and findings:
1) We developed a circuit model of the human primary visual cortex with two cortical layers (corresponding to the superficial and middle cortical layers), that respects key known features of the biological circuitry in the cortex. Activities of neurons in the model's superficial layer were read to output a perceptual decision. We then asked what is the optimal way of modifying the network's excitatory and inhibitory connectivity, in each layer, to enhance perceptual discrimination without disturbing the biological equilibrium of the cortex (e.g. without causing seizure-like runaway excitation). 
2) We found that such optimal training robustly led to a strengthening of inhibitory connectivity and weakening of excitatory connections, in line with experimental findings. Further, these changes were stronger and more robust in the superficial layer compared to the middle layer. 
3) We also found that, as a result of optimal training, the information content of neural activity patterns about the stimulus increased significantly more in the superficial layer, again in agreement with the experimental finding. 
4) Given the mechanistic nature of the model, we were able to perform ablations of various circuit features to shed light on the role played by them in determining the above outcomes. For example, it had been hypothesized that improvements in neural representation are primarily manifesting in the superficial layers because of the long-range excitatory connectivity in those layers. By ablations of this feature as well as the location of the readout in the model, we found that the emergence of feedforward (readout) connections from the superficial layer, as in the real cortex, is more important than that layer's long-range connectivity in focusing changes in neural representations to this layer.

In summary, our model explains observed changes in cortical connectivity and activity patterns as arising from an optimal trade-off between improvement in task performance and maintenance of biological equilibrium. It also sheds light on the role played by key structural features of the cortical circuit in shaping the changes in excitatory/inhibitory connectivity and neural representations. In the near future, we aim to apply our model to a different class of perceptual tasks, training in which has been observed to lead to opposite changes in cortical excitation and inhibition; we will test whether the model can also explain those opposite changes as arising from the same computational principles.
Exploitation Route The developed model, and the code package (for model simulations and its gradient-based training) which has been published, can be used by other neuroscientists to parsimoniously model phenomena involving the human cotex. For example to formulate hypotheses about the role of different cortical circuit features in phenomena such as perceptual learning and visual adaptation. Given the mechanistic nature of the model, such hypotheses can include predictions about the role of different interventions (such as pharmacological interventions or electrical stimulations) on perceptual learning, or in improving visual perception.
Sectors Healthcare

Pharmaceuticals and Medical Biotechnology

URL https://2024.ccneuro.org/poster/?id=187
 
Title JAX-based package for simulation and training of the SSN cortical network model 
Description We have implemented and are using a user-friendly package for simulations of the Stabilized Supralinear Network (SSN) model, that is based on JAX, a Python library that enables GPU-based high-performance computing via a streamlined API. The SSN is a model of cortical circuitry, which incorporates key biological features of those circuits, and has successfully accounted for a range of nonlinear cortical response properties. 
Type Of Material Computer model/algorithm 
Year Produced 2024 
Provided To Others? Yes  
Impact By allowing an easy to use (almost plug-and-play) gradient-based optimization of the SSN model's circuit parameters, this package allows us and others (as we will publicly share our package once the first publication from this project is submitted) to integrate the SSN biological network into AI and deep learning related projects. The package would also simplify the generalization (via inhertiance of network classes) to other network model types. 
URL https://github.com/monikajozsa/SSN-VisualCortex
 
Title Research data supporting: "Recurrent inhibition refines mental templates to optimize perceptual decisions". 
Description Data for "Recurrent inhibition refines mental templates to optimize perceptual decisions". For more details, please see attached file: 'Description of uploaded data.docx' 
Type Of Material Database/Collection of data 
Year Produced 2024 
Provided To Others? Yes  
Impact N/A 
URL https://www.repository.cam.ac.uk/handle/1810/368906
 
Description BBC News: Brain Hacks 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Broadcast from the BBC. Synopsis: "How do we keep our brains healthy? And is there anything we can do to help strengthen crucial connections and keep our minds younger in the process? Science journalist Melissa Hogenboom sets out to understand more about the brain's capacity to respond to change, helping us to learn and to heal. She looks at the most cutting-edge scientific research and has her own brain scanned and analysed, with intriguing results."
Year(s) Of Engagement Activity 2023
URL https://www.bbc.co.uk/iplayer/episode/m001qr3k/brain-hacks
 
Description Brainwaves for Learning - Cambridge ReseARch trail, Cambridge Science Festival 2024 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact The interdisciplinary Cambridge Festival takes place each March with a mixture of on online, on-demand and in-person events covering all aspects of the world-leading research happening at Cambridge University. This was a new augmented reality trail showcasing the world leading research of the University of Cambridge in a new light.
Year(s) Of Engagement Activity 2024
URL https://www.cam.ac.uk/stories/cambridge-ar-trail
 
Description Cambridge Science Festival 2023 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact The interdisciplinary Cambridge Festival takes place each March with a mixture of on online, on-demand and in-person events covering all aspects of the world-leading research happening at Cambridge University
Year(s) Of Engagement Activity 2023
URL https://www.festival.cam.ac.uk/