Learn to integrate parts for whole through correlated neural variability (2401.00746v1)
Abstract: Sensory perception originates from the responses of sensory neurons, which react to a collection of sensory signals linked to various physical attributes of a singular perceptual object. Unraveling how the brain extracts perceptual information from these neuronal responses is a pivotal challenge in both computational neuroscience and machine learning. Here we introduce a statistical mechanical theory, where perceptual information is first encoded in the correlated variability of sensory neurons and then reformatted into the firing rates of downstream neurons. Applying this theory, we illustrate the encoding of motion direction using neural covariance and demonstrate high-fidelity direction recovery by spiking neural networks. Networks trained under this theory also show enhanced performance in classifying natural images, achieving higher accuracy and faster inference speed. Our results challenge the traditional view of neural covariance as a secondary factor in neural coding, highlighting its potential influence on brain function.
- Ackels, T. et al. Fast odour dynamics are encoded in the olfactory system and guide behaviour. Nature 593, 558–563 (2021).
- Caruso, V. C. et al. Single neurons may encode simultaneous stimuli by switching between activity patterns. Nature Communications 9 (2018).
- Temporal limits of visual motion processing: Psychophysics and neurophysiology. Vision 3, 5 (2019).
- Sensory neural codes using multiplexed temporal scales. Trends in Neurosciences 33, 111–120 (2010).
- Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. The Journal of Physiology 160, 106–154 (1962).
- An evaluation of the two-dimensional gabor filter model of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 1233–1258 (1987).
- Emergence of simple-cell receptive field properties by learning a sparse code for natural images. Nature 381, 607–609 (1996).
- Deep learning. Nature 521, 436–444 (2015).
- Neuroscience-inspired artificial intelligence. Neuron 95, 245–258 (2017).
- Deep supervised, but not unsupervised, models may explain it cortical representation. Plos Computational Biology 10, e1003915 (2014).
- Comparison of deep neural networks to spatio-temporal cortical dynamics of human visual object recognition reveals hierarchical correspondence. Scientific Reports 6 (2016).
- Li, Y. et al. Dissecting neural computations in the human auditory pathway using deep neural networks for speech. Nature Neuroscience (2023).
- Neuronal variability: non-stationary responses to identical visual stimuli. Brain Research 79, 405–418 (1974).
- The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Research 23, 775–785 (1983).
- The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. The Journal of Neuroscience 13, 334–350 (1993).
- Integrator or coincidence detector? the role of the cortical neuron revisited. Trends in Neurosciences 19, 130–137 (1996).
- Cracking the neural code for sensory perception by combining statistics, intervention, and behavior. Neuron 93, 491–507 (2017).
- Golledge, H. D. R. et al. Correlations, feature-binding and population coding in primary visual cortex. NeuroReport 14, 1045–1050 (2003).
- The role of correlations in direction and contrast coding in the primary visual cortex. The Journal of Neuroscience 27, 2338–2348 (2007).
- The neuronal encoding of information in the brain. Progress in Neurobiology 95, 448–490 (2011).
- Nonlinear population codes. Neural Computation 16, 1105–1136 (2004).
- Effects of noise correlations on information encoding and decoding. Journal of Neurophysiology 95, 3633–3644 (2006).
- Pillow, J. W. et al. Spatio-temporal correlations and visual signalling in a complete neuronal population. Nature 454, 995–999 (2008).
- El-Gaby, M. et al. An emergent neural coactivity code for dynamic memory. Nature Neuroscience 24, 694–704 (2021).
- The structures and functions of correlations in neural population codes. Nature Reviews Neuroscience 23, 551–567 (2022).
- An exact method to quantify the information transmitted by different mechanisms of correlational coding. Network: Computation in Neural Systems 14, 35–60 (2003).
- Synergy, redundancy, and independence in population codes. The Journal of Neuroscience 23, 11539–11553 (2003).
- Principles of neural coding (CRC Press, 2013).
- Untangling invariant object recognition. Trends in Cognitive Sciences 11, 333–341 (2007).
- How does the brain solve visual object recognition? Neuron 73, 415–434 (2012).
- Dynamics of moment neuronal networks. Physical Review E 73, 041906 (2006).
- On a gaussian neuronal field model. NeuroImage 52, 913–933 (2010).
- Qi, Y. et al. Toward spike-based stochastic neural computing (2023). 2305.13982.
- Orientation selectivity in the cat’s striate cortex is invariant with stimulus contrast. Experimental Brain Research 46, 457–461 (1982).
- Kohn, A. Stimulus dependence of neuronal correlation in primary visual cortex of the macaque. Journal Of Neuroscience 25, 3661–3673 (2005).
- Temporal encoding in nervous systems: A rigorous definition. Journal of Computational Neuroscience 2, 149–162 (1995).
- Correlation between neural spike trains increases with firing rate. Nature 448, 802–806 (2007).
- Bayesian inference with probabilistic population codes. Nature Neuroscience 9, 1432–1438 (2006).
- Neural correlations, population coding and computation. Nature Reviews Neuroscience 7, 358–366 (2006).
- Neural tuning and representational geometry. Nature Reviews Neuroscience 22, 703–718 (2021).
- The caltech-ucsd birds-200-2011 dataset. Tech. Rep. CNS-TR-2011-001 (2011).
- Wei, X.-S. et al. Fine-grained image analysis with deep learning: A survey. IEEE Transactions on Pattern Analysis and Machine Intelligence 44, 8927–8948 (2022).
- Very deep convolutional networks for large-scale image recognition. Arxiv Preprint Arxiv:1409.1556 (2014).
- Deep cnns meet global covariance pooling: Better representation and generalization. IEEE Transactions on Pattern Analysis and Machine Intelligence 1–1 (2020).
- On the eigenvalues of global covariance pooling for fine-grained visual recognition. IEEE Transactions on Pattern Analysis and Machine Intelligence 1–1 (2022).
- Combinatorial receptor codes for odors. Cell 96, 713–723 (1999).
- The neural basis for combinatorial coding in a cortical population response. The Journal of Neuroscience 28, 13522–13531 (2008).
- Piasini, E. et al. Temporal stability of stimulus representation increases along rodent visual cortical hierarchies. Nature Communications 12, 4448 (2021).
- Siegle, J. H. et al. Survey of spiking in the mouse visual system reveals functional hierarchy. Nature 592, 86–92 (2021).
- Burst-dependent synaptic plasticity can coordinate learning in hierarchical circuits. Nature Neuroscience 24, 1010–1019 (2021).