Synaptic Learning Rules and Sparse Coding in a Model Sensory System

Neural circuits exploit numerous strategies for encoding information. Although the functional significance of individual coding mechanisms has been investigated, ways in which multiple mechanisms interact and integrate are not well understood. The locust olfactory system, in which dense, transiently synchronized spike trains across ensembles of antenna lobe (AL) neurons are transformed into a sparse representation in the mushroom body (MB; a region associated with memory), provides a well-studied preparation for investigating the interaction of multiple coding mechanisms. Recordings made in vivo from the insect MB demonstrated highly specific responses to odors in Kenyon cells (KCs). Typically, only a few KCs from the recorded population of neurons responded reliably when a specific odor was presented. Different odors induced responses in different KCs. Here, we explored with a biologically plausible model the possibility that a form of plasticity may control and tune synaptic weights of inputs to the mushroom body to ensure the specificity of KCs' responses to familiar or meaningful odors. We found that plasticity at the synapses between the AL and the MB efficiently regulated the delicate tuning necessary to selectively filter the intense AL oscillatory output and condense it to a sparse representation in the MB. Activity-dependent plasticity drove the observed specificity, reliability, and expected persistence of odor representations, suggesting a role for plasticity in information processing and making a testable prediction about synaptic plasticity at AL-MB synapses.

[1]  G. Laurent,et al.  Encoding of Olfactory Information with Oscillating Neural Assemblies , 1994, Science.

[2]  R. Traub,et al.  Neuronal Networks of the Hippocampus , 1991 .

[3]  Daniel D. Lee,et al.  Equilibrium properties of temporally asymmetric Hebbian plasticity. , 2000, Physical review letters.

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

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

[6]  Bruno A Olshausen,et al.  Sparse coding of sensory inputs , 2004, Current Opinion in Neurobiology.

[7]  Wulfram Gerstner,et al.  A neuronal learning rule for sub-millisecond temporal coding , 1996, Nature.

[8]  Nicholas T. Carnevale,et al.  The NEURON Simulation Environment , 1997, Neural Computation.

[9]  K D Miller,et al.  Models of activity-dependent neural development. , 1992, Progress in brain research.

[10]  D. Debanne,et al.  Cooperative interactions in the induction of long-term potentiation and depression of synaptic excitation between hippocampal CA3-CA1 cell pairs in vitro. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Terrence J. Sejnowski,et al.  Model of Cellular and Network Mechanisms for Odor-Evoked Temporal Patterning in the Locust Antennal Lobe , 2001, Neuron.

[12]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[13]  P. Schwindt,et al.  Synaptic depression in the localization of sound , 2003, Nature.

[14]  G. Laurent,et al.  Intrinsic and Circuit Properties Favor Coincidence Detection for Decoding Oscillatory Input , 2004, The Journal of Neuroscience.

[15]  K. I. Blum,et al.  Functional significance of long-term potentiation for sequence learning and prediction. , 1996, Cerebral cortex.

[16]  G. Laurent,et al.  Distinct Mechanisms for Synchronization and Temporal Patterning of Odor-Encoding Neural Assemblies , 1996, Science.

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

[18]  G. Laurent,et al.  Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts , 2007, Nature.

[19]  T. Sejnowski,et al.  Network Oscillations: Emerging Computational Principles , 2006, The Journal of Neuroscience.

[20]  Wolfgang Rössler,et al.  F‐actin at identified synapses in the mushroom body neuropil of the insect brain , 2004, The Journal of comparative neurology.

[21]  S. Wang,et al.  Graded bidirectional synaptic plasticity is composed of switch-like unitary events. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Christoph Braun,et al.  Coherence of gamma-band EEG activity as a basis for associative learning , 1999, Nature.

[23]  M. Stryker,et al.  The role of visual experience in the development of columns in cat visual cortex. , 1998, Science.

[24]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[25]  D. Debanne,et al.  Heterogeneity of Synaptic Plasticity at Unitary CA3–CA1 and CA3–CA3 Connections in Rat Hippocampal Slice Cultures , 1999, The Journal of Neuroscience.

[26]  J. Hopfield,et al.  All-or-none potentiation at CA3-CA1 synapses. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Kenneth D. Miller,et al.  The Role of Constraints in Hebbian Learning , 1994, Neural Computation.

[28]  G. Laurent,et al.  Short-term memory in olfactory network dynamics , 1999, Nature.

[29]  Ronald L. Davis Mushroom bodies and drosophila learning , 1993, Neuron.

[30]  L. Luo,et al.  Representation of the Glomerular Olfactory Map in the Drosophila Brain , 2002, Cell.

[31]  Karel Svoboda,et al.  Stereotyped Odor-Evoked Activity in the Mushroom Body of Drosophila Revealed by Green Fluorescent Protein-Based Ca2+ Imaging , 2004, The Journal of Neuroscience.

[32]  G. Laurent,et al.  Transient Dynamics versus Fixed Points in Odor Representations by Locust Antennal Lobe Projection Neurons , 2005, Neuron.

[33]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

[34]  G. Laurent,et al.  Odour encoding by temporal sequences of firing in oscillating neural assemblies , 1996, Nature.

[35]  T. Sejnowski,et al.  Fast Odor Learning Improves Reliability of Odor Responses in the Locust Antennal Lobe , 2005, Neuron.

[36]  M. Heisenberg What do the mushroom bodies do for the insect brain? an introduction. , 1998, Learning & memory.

[37]  Lawrence C Katz,et al.  Ocular dominance development revisited , 2002, Current Opinion in Neurobiology.

[38]  Ronald L. Davis,et al.  Spatiotemporal Rescue of Memory Dysfunction in Drosophila , 2003, Science.

[39]  T. Sejnowski,et al.  Storing covariance with nonlinearly interacting neurons , 1977, Journal of mathematical biology.

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

[41]  G. Laurent,et al.  Impaired odour discrimination on desynchronization of odour-encoding neural assemblies , 1997, Nature.

[42]  D. O'Dowd,et al.  Fast Synaptic Currents in Drosophila Mushroom Body Kenyon Cells Are Mediated by α-Bungarotoxin-Sensitive Nicotinic Acetylcholine Receptors and Picrotoxin-Sensitive GABA Receptors , 2003, The Journal of Neuroscience.

[43]  D. Tolhurst,et al.  Characterizing the sparseness of neural codes , 2001, Network.

[44]  Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory , 2022 .

[45]  Alan Gelperin,et al.  Olfactory Computations and Network Oscillation , 2006, The Journal of Neuroscience.

[46]  Wulfram Gerstner,et al.  Intrinsic Stabilization of Output Rates by Spike-Based Hebbian Learning , 2001, Neural Computation.

[47]  Alan Gelperin,et al.  Olfactory Computations and Network Oscillations , 2006 .

[48]  Bradley L. Schlaggar,et al.  Postsynaptic control of plasticity in developing somatosensory cortex , 1993, Nature.

[49]  T. Sejnowski,et al.  Model of Transient Oscillatory Synchronization in the Locust Antennal Lobe , 2001, Neuron.

[50]  D. Tank,et al.  Odour-modulated collective network oscillations of olfactory interneurons in a terrestrial mollusc , 1990, Nature.

[51]  Linda B Buck,et al.  Odor maps in the olfactory cortex. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Gene E. Robinson,et al.  Experience- and Age-Related Outgrowth of Intrinsic Neurons in the Mushroom Bodies of the Adult Worker Honeybee , 2001, The Journal of Neuroscience.

[53]  L. Abbott,et al.  Competitive Hebbian learning through spike-timing-dependent synaptic plasticity , 2000, Nature Neuroscience.

[54]  W. Singer Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[55]  R. Menzel,et al.  Neural plasticity of mushroom body-extrinsic neurons in the honeybee brain , 2005, Journal of Experimental Biology.

[56]  Kei Ito,et al.  Integration of Chemosensory Pathways in the Drosophila Second-Order Olfactory Centers , 2004, Current Biology.

[57]  D. Debanne,et al.  Long‐term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures , 1998, The Journal of physiology.

[58]  J. Leo van Hemmen,et al.  Modeling Synaptic Plasticity in Conjunction with the Timing of Pre- and Postsynaptic Action Potentials , 2000, Neural Computation.

[59]  L. Abbott,et al.  Cortical Development and Remapping through Spike Timing-Dependent Plasticity , 2001, Neuron.

[60]  R. Johansson,et al.  First spikes in ensembles of human tactile afferents code complex spatial fingertip events , 2004, Nature Neuroscience.

[61]  Gilles Laurent,et al.  A Simple Connectivity Scheme for Sparse Coding in an Olfactory System , 2007, The Journal of Neuroscience.

[62]  G. Laurent,et al.  Temporal Representations of Odors in an Olfactory Network , 1996, The Journal of Neuroscience.

[63]  Mark C. W. van Rossum,et al.  Stable Hebbian Learning from Spike Timing-Dependent Plasticity , 2000, The Journal of Neuroscience.

[64]  L. Abbott,et al.  Cascade Models of Synaptically Stored Memories , 2005, Neuron.

[65]  D. Feldman,et al.  Long-term depression induced by sensory deprivation during cortical map plasticity in vivo , 2003, Nature Neuroscience.

[66]  P. J. Sjöström,et al.  Rate, Timing, and Cooperativity Jointly Determine Cortical Synaptic Plasticity , 2001, Neuron.

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

[68]  T. Sejnowski,et al.  Thalamocortical oscillations in the sleeping and aroused brain. , 1993, Science.

[69]  L. Abbott,et al.  Synaptic plasticity: taming the beast , 2000, Nature Neuroscience.

[70]  G. Laurent,et al.  Adaptive regulation of sparseness by feedforward inhibition , 2007, Nature Neuroscience.