Evolving super stimuli for real neurons using deep generative networks

Finding the best stimulus for a neuron is challenging because it is impossible to test all possible stimuli. Here we used a vast, unbiased, and diverse hypothesis space encoded by a generative deep neural network model to investigate neuronal selectivity in inferotemporal cortex without making any assumptions about natural features or categories. A genetic algorithm, guided by neuronal responses, searched this space for optimal stimuli. Evolved synthetic images evoked higher firing rates than even the best natural images and revealed diagnostic features, independently of category or feature selection. This approach provides a way to investigate neural selectivity in any modality that can be represented by a neural network and challenges our understanding of neural coding in visual cortex. Highlights A generative deep neural network interacted with a genetic algorithm to evolve stimuli that maximized the firing of neurons in alert macaque inferotemporal and primary visual cortex. The evolved images activated neurons more strongly than did thousands of natural images. Distance in image space from the evolved images predicted responses of neurons to novel images.

[1]  J. P. Jones,et al.  The two-dimensional spatial structure of simple receptive fields in cat striate cortex. , 1987, Journal of neurophysiology.

[2]  M. Giese,et al.  Norm-based face encoding by single neurons in the monkey inferotemporal cortex , 2006, Nature.

[3]  C. R. Michael Color vision mechanisms in monkey striate cortex: simple cells with dual opponent-color receptive fields. , 1978, Journal of neurophysiology.

[4]  Sabine Kastner,et al.  Neurons with radial receptive fields in monkey area V4A: evidence of a subdivision of prelunate gyrus based on neuronal response properties , 2002, Experimental Brain Research.

[5]  Minami Ito,et al.  Size and position invariance of neuronal responses in monkey inferotemporal cortex. , 1995, Journal of neurophysiology.

[6]  S. Zeki Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey , 1974, The Journal of physiology.

[7]  Eric T. Carlson,et al.  A neural code for three-dimensional object shape in macaque inferotemporal cortex , 2008, Nature Neuroscience.

[8]  D. Perrett,et al.  Visual neurones responsive to faces in the monkey temporal cortex , 2004, Experimental Brain Research.

[9]  S. Zeki,et al.  Colour coding in the superior temporal sulcus of rhesus monkey visual cortex , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[10]  Eero P. Simoncelli,et al.  A Parametric Texture Model Based on Joint Statistics of Complex Wavelet Coefficients , 2000, International Journal of Computer Vision.

[11]  R. Desimone,et al.  Stimulus-selective properties of inferior temporal neurons in the macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  D. B. Bender,et al.  Visual properties of neurons in inferotemporal cortex of the Macaque. , 1972, Journal of neurophysiology.

[13]  D. Hubel Single unit activity in striate cortex of unrestrained cats , 1959, The Journal of physiology.

[14]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

[15]  Thomas Brox,et al.  Generating Images with Perceptual Similarity Metrics based on Deep Networks , 2016, NIPS.

[16]  Tomaso Poggio,et al.  Trade-Off between Object Selectivity and Tolerance in Monkey Inferotemporal Cortex , 2007, The Journal of Neuroscience.

[17]  D. Hubel,et al.  Complex–unoriented cells in a subregion of primate area 18 , 1985, Nature.

[18]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[19]  Keiji Tanaka,et al.  Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. , 1994, Journal of neurophysiology.

[20]  Elias B. Issa,et al.  Precedence of the Eye Region in Neural Processing of Faces , 2012, The Journal of Neuroscience.

[21]  Thomas Brox,et al.  Synthesizing the preferred inputs for neurons in neural networks via deep generator networks , 2016, NIPS.

[22]  Michael S. Bernstein,et al.  ImageNet Large Scale Visual Recognition Challenge , 2014, International Journal of Computer Vision.

[23]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[24]  G. Griffin,et al.  Caltech-256 Object Category Dataset , 2007 .

[25]  D. Pollen,et al.  Space-time spectra of complex cell filters in the macaque monkey: A comparison of results obtained with pseudowhite noise and grating stimuli , 1994, Visual Neuroscience.

[26]  D. J. Felleman,et al.  Receptive field properties of neurons in area V3 of macaque monkey extrastriate cortex. , 1987, Journal of neurophysiology.

[27]  Li Fei-Fei,et al.  ImageNet: A large-scale hierarchical image database , 2009, CVPR.

[28]  S. Zeki,et al.  Colour coding in rhesus monkey prestriate cortex. , 1973, Brain research.

[29]  Doris Y. Tsao,et al.  A face feature space in the macaque temporal lobe , 2009, Nature Neuroscience.

[30]  C. Connor,et al.  Responses to contour features in macaque area V4. , 1999, Journal of neurophysiology.

[31]  C. Blakemore,et al.  The neural mechanism of binocular depth discrimination , 1967, The Journal of physiology.

[32]  Ha Hong,et al.  Performance-optimized hierarchical models predict neural responses in higher visual cortex , 2014, Proceedings of the National Academy of Sciences.

[33]  Doris Y. Tsao,et al.  The Code for Facial Identity in the Primate Brain , 2017, Cell.

[34]  G. Bellala,et al.  Parametric Texture Model based on Joint Statistics , 2009 .