Stimulus space complexity determines the ratio of specialist and generalist neurons during pattern recognition

Abstract Neural processing layers built on divergent connectivity patterns display two types of stimulus-dependent responses: neurons that react to a few stimuli, specialists, and other ones that respond to a wide range of inputs, generalists. Specialists are essential for the discrimination of stimuli and generalists extract common and generic properties from them. This neural heterogeneity could have emerged because of animal adaptation to the environment. Thus, we suggest that there is a relationship between the percentage of specialists and generalists and the stimulus complexity. In order to study this possible relationship, we use patterns with different complexities in a bio-inspired neural network and calculate their classification errors for different ratios of these types of neurons. This study shows that, when the complexity of the stimuli is low, the minimum classification error is achieved with almost any specialist-generalist ratio. Thus, in this case, the role of these neurons during pattern recognition is unspecific. When this complexity is intermediate, both are needed to minimize the classification error, usually in a similar proportion. For increasing stimulus complexity, the importance of generalists decreases, until their relevance is fully nullified when the complexity is high. Therefore, if we adjust the specialist-generalist ratio to the complexity of patterns, we can build more effective neural networks for pattern recognition. Finally, we propose an estimation of stimulus complexity based on the proportion of these types of neurons observed by neural recordings. This offers the possibility to evaluate the stimulus complexity to which animals are adapted.

[1]  Emilio Salinas,et al.  Gain Modulation A Major Computational Principle of the Central Nervous System , 2000, Neuron.

[2]  T. Baker,et al.  Odour-plume dynamics influence the brain's olfactory code , 2001, Nature.

[3]  Shankar Vembu,et al.  Chemical gas sensor drift compensation using classifier ensembles , 2012 .

[4]  Ramón Huerta,et al.  Fast and Robust Learning by Reinforcement Signals: Explorations in the Insect Brain , 2009, Neural Computation.

[5]  Gilles Laurent,et al.  Olfactory network dynamics and the coding of multidimensional signals , 2002, Nature Reviews Neuroscience.

[6]  B. Smith,et al.  Different thresholds for detection and discrimination of odors in the honey bee (Apis mellifera). , 2004, Chemical senses.

[7]  Ramón Huerta,et al.  Analysis of perfect mappings of the stimuli through neural temporal sequences , 2004, Neural Networks.

[8]  Dominique Martinez,et al.  Competition-Based Model of Pheromone Component Ratio Detection in the Moth , 2011, PloS one.

[9]  M Heisenberg,et al.  Tissue-specific expression of a type I adenylyl cyclase rescues the rutabaga mutant memory defect: in search of the engram. , 2000, Learning & memory.

[10]  R. Menzel,et al.  Associative learning modifies neural representations of odors in the insect brain , 1999, Nature Neuroscience.

[11]  Eduardo Serrano,et al.  Gain Control Network Conditions in Early Sensory Coding , 2013, PLoS Comput. Biol..

[12]  Silke Sachse,et al.  The coding of odour‐intensity in the honeybee antennal lobe: local computation optimizes odour representation , 2003, The European journal of neuroscience.

[13]  Francisco B. Rodríguez,et al.  Specialist Neurons in Feature Extraction Are Responsible for Pattern Recognition Process in Insect Olfaction , 2015, IWINAC.

[14]  M. Chacron,et al.  Neural heterogeneities and stimulus properties affect burst coding in vivo , 2010, Neuroscience.

[15]  Glenn C. Turner,et al.  Oscillations and Sparsening of Odor Representations in the Mushroom Body , 2002, Science.

[16]  R. Huerta,et al.  Neural Sensitivity to Odorants in Deprived and Normal Olfactory Bulbs , 2013, PloS one.

[17]  B. Smith,et al.  Impairment of olfactory discrimination by blockade of GABA and nitric oxide activity in the honey bee antennal lobes. , 2000 .

[18]  Roberto Malinow,et al.  Genetic Manipulation of the Odor-Evoked Distributed Neural Activity in the Drosophila Mushroom Body , 2001, Neuron.

[19]  Lonneke B. M. Eeuwes,et al.  Efficient Encoding of Vocalizations in the Auditory Midbrain , 2010, The Journal of Neuroscience.

[20]  Francisco B. Rodríguez,et al.  Neural Trade-Offs among Specialist and Generalist Neurons in Pattern Recognition , 2014, EANN.

[21]  Randall C. O'Reilly,et al.  Generalization in Interactive Networks: The Benefits of Inhibitory Competition and Hebbian Learning , 2001, Neural Computation.

[22]  J. Loon,et al.  Specialist deterrent chemoreceptors enable Pieris caterpillars to discriminate between chemically different deterrents , 1999 .

[23]  Tim Tully,et al.  Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory , 2001, Nature.

[24]  Ramón Huerta,et al.  Learning Classification in the Olfactory System of Insects , 2004, Neural Computation.

[25]  Troy Zars,et al.  Behavioral functions of the insect mushroom bodies , 2000, Current Opinion in Neurobiology.

[26]  Randolf Menzel,et al.  Probing the olfactory code , 2000, Nature Neuroscience.

[27]  G. Laurent A systems perspective on early olfactory coding. , 1999, Science.

[28]  R. Fisher THE USE OF MULTIPLE MEASUREMENTS IN TAXONOMIC PROBLEMS , 1936 .

[29]  Alexander Vergara,et al.  On the calibration of sensor arrays for pattern recognition using the minimal number of experiments , 2014 .

[30]  M. Frank,et al.  The organization of taste sensibilities in hamster chorda tympani nerve fibers , 1988, The Journal of general physiology.

[31]  G. Laurent,et al.  GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system , 1996, The Journal of comparative neurology.

[32]  G. Laurent Dynamical representation of odors by oscillating and evolving neural assemblies , 1996, Trends in Neurosciences.

[33]  Randolf Menzel,et al.  Sensory Memory for Odors Is Encoded in Spontaneous Correlated Activity Between Olfactory Glomeruli , 2006, Neural Computation.

[34]  W. Bialek,et al.  The Neural Basis for Combinatorial Coding in a Cortical Population Response , 2008, The Journal of Neuroscience.

[35]  Francisco B. Rodríguez,et al.  Exploring a Mathematical Model of Gain Control via Lateral Inhibition in the Antennal Lobe , 2017, IWANN.

[36]  T. Christensen,et al.  Making scents out of spatial and temporal codes in specialist and generalist olfactory networks. , 2005, Chemical senses.

[37]  Gilles Laurent,et al.  Transformation of Olfactory Representations in the Drosophila Antennal Lobe , 2004, Science.

[38]  L. C. Katz,et al.  Optical Imaging of Odorant Representations in the Mammalian Olfactory Bulb , 1999, Neuron.

[39]  R. Menzel,et al.  A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy , 1999, Cell and Tissue Research.

[40]  Nirav C. Merchant,et al.  Flybrain, an on-line atlas and database of the Drosophila nervous system , 1995, Neuron.

[41]  Shawn R. Olsen,et al.  Lateral presynaptic inhibition mediates gain control in an olfactory circuit , 2008, Nature.

[42]  R. Lundy,et al.  Gustatory neuron types in rat geniculate ganglion. , 1999, Journal of neurophysiology.

[43]  R. Davis,et al.  The Role of Drosophila Mushroom Body Signaling in Olfactory Memory , 2001, Science.

[44]  Randolf Menzel,et al.  A semi-in-vivo preparation for optical recording of the insect brain , 1997, Journal of Neuroscience Methods.

[45]  M. Chacron,et al.  Neural heterogeneities influence envelope and temporal coding at the sensory periphery , 2011, Neuroscience.

[46]  Kevin C. Daly,et al.  Detailed Characterization of Local Field Potential Oscillations and Their Relationship to Spike Timing in the Antennal Lobe of the Moth Manduca sexta , 2011, Front. Neuroeng..

[47]  A. Keller,et al.  Humans Can Discriminate More than 1 Trillion Olfactory Stimuli , 2014, Science.

[48]  Glenn C. Turner,et al.  Olfactory representations by Drosophila mushroom body neurons. , 2008, Journal of neurophysiology.

[49]  Wanhe Li,et al.  Imaging a Population Code for Odor Identity in the Drosophila Mushroom Body , 2013, The Journal of Neuroscience.

[50]  B. Smith,et al.  Learning-based recognition and discrimination of floral odors , 2005 .

[51]  U. Kaupp Olfactory signalling in vertebrates and insects: differences and commonalities , 2010, Nature Reviews Neuroscience.

[52]  G. Shepherd,et al.  Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. , 1997, Annual review of neuroscience.

[53]  André Longtin,et al.  Differential effects of excitatory and inhibitory heterogeneity on the gain and asynchronous state of sparse cortical networks , 2014, Front. Comput. Neurosci..

[54]  N. Strausfeld,et al.  Development of laminar organization in the mushroom bodies of the cockroach: Kenyon cell proliferation, outgrowth, and maturation , 2001, The Journal of comparative neurology.

[55]  Glenn C. Turner,et al.  Integration of the olfactory code across dendritic claws of single mushroom body neurons , 2013, Nature Neuroscience.

[56]  N. Strausfeld,et al.  Evolution, discovery, and interpretations of arthropod mushroom bodies. , 1998, Learning & memory.

[57]  N. Strausfeld,et al.  Mushroom bodies of the cockroach: Their participation in place memory , 1998, The Journal of comparative neurology.

[58]  C. Gallistel,et al.  The learning curve: implications of a quantitative analysis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[59]  V. Jayaraman,et al.  Intensity versus Identity Coding in an Olfactory System , 2003, Neuron.

[60]  M Heisenberg,et al.  Localization of a short-term memory in Drosophila. , 2000, Science.

[61]  R. Huerta,et al.  A Computational Framework for Understanding Decision Making through Integration of Basic Learning Rules , 2013, The Journal of Neuroscience.

[62]  R. Menzel,et al.  Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera , 2001, The Journal of comparative neurology.

[63]  B. Kimmerle,et al.  Physiological and morphological characterization of honeybee olfactory neurons combining electrophysiology, calcium imaging and confocal microscopy , 2003, Journal of Comparative Physiology A.

[64]  P. Mahalanobis On the generalized distance in statistics , 1936 .

[65]  P. Rousseeuw Silhouettes: a graphical aid to the interpretation and validation of cluster analysis , 1987 .

[66]  Ina Frambach,et al.  GABAergic synaptic connections in mushroom bodies of insect brains. , 2008, Acta biologica Hungarica.

[67]  Ramón Huerta,et al.  Design Parameters of the Fan-Out Phase of Sensory Systems , 2003, Journal of Computational Neuroscience.

[68]  M. Frank,et al.  Neuron types, receptors, behavior, and taste quality , 2000, Physiology & Behavior.

[69]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[70]  G. Edelman,et al.  Consciousness and Complexity , 1998 .

[71]  Francisco B. Rodríguez,et al.  Regulation of specialists and generalists by neural variability improves pattern recognition performance , 2015, Neurocomputing.

[72]  N. Strausfeld Organization of the honey bee mushroom body: Representation of the calyx within the vertical and gamma lobes , 2002, The Journal of comparative neurology.

[73]  Francisco B. Rodríguez,et al.  Neuron Threshold Variability in an Olfactory Model Improves Odorant Discrimination , 2013, IWINAC.

[74]  M. Bitterman,et al.  Classical conditioning of proboscis extension in honeybees (Apis mellifera). , 1983, Journal of comparative psychology.

[75]  M. I. Rabinovich,et al.  Dynamical coding of sensory information with competitive networks , 2000, Journal of Physiology-Paris.

[76]  Francisco B. Rodríguez,et al.  Techniques for temporal detection of neural sensitivity to external stimulation , 2009, Biological Cybernetics.

[77]  Leonard Maler,et al.  Neural heterogeneity and efficient population codes for communication signals. , 2010, Journal of neurophysiology.

[78]  L. M. Schoonhoven,et al.  Specialist deterrent chemoreceptors enable Pieris butterflies to discriminate chemically different deterrents. , 1998 .

[79]  Tin Kam Ho,et al.  Complexity Measures of Supervised Classification Problems , 2002, IEEE Trans. Pattern Anal. Mach. Intell..

[80]  N. Strausfeld,et al.  The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. , 1998, Learning & memory.

[81]  T. R. Tobin,et al.  Conditional withholding of proboscis extension in honeybees (Apis mellifera) during discriminative punishment. , 1991 .

[82]  Peter Dayan,et al.  Bee foraging in uncertain environments using predictive hebbian learning , 1995, Nature.