Synaptic pathways in neural microcircuits

The functions performed by different neural microcircuits depend on the anatomical and physiological properties of the various synaptic pathways connecting neurons. Neural microcircuits across various species and brain regions are similar in terms of their repertoire of neurotransmitters, their synaptic kinetics, their short-term and long-term plasticity, and the target-specificity of their synaptic connections. However, microcircuits can be fundamentally different in terms of the precise recurrent design used to achieve a specific functionality. In this review, which is part of the TINS Microcircuits Special Feature, we compare the connectivity designs in spinal, hippocampal, neocortical and cerebellar microcircuits, and discuss the different computational challenges that each microcircuit faces.

[1]  S. Nelson,et al.  Short-Term Depression at Thalamocortical Synapses Contributes to Rapid Adaptation of Cortical Sensory Responses In Vivo , 2002, Neuron.

[2]  H. Markram,et al.  Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. , 2002, Cerebral cortex.

[3]  M. J. Friedlander,et al.  The time course and amplitude of EPSPs evoked at synapses between pairs of CA3/CA1 neurons in the hippocampal slice , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  Henry Markram,et al.  Real-Time Computing Without Stable States: A New Framework for Neural Computation Based on Perturbations , 2002, Neural Computation.

[5]  J. Deuchars,et al.  CA1 pyramid-pyramid connections in rat hippocampus in vitro: Dual intracellular recordings with biocytin filling , 1996, Neuroscience.

[6]  S. Grillner,et al.  Substance P Modulates NMDA Responses and Causes Long-Term Protein Synthesis-Dependent Modulation of the Lamprey Locomotor Network , 1998, The Journal of Neuroscience.

[7]  S. Grillner,et al.  The activity‐dependent plasticity of segmental and intersegmental synaptic connections in the lamprey spinal cord , 2000, The European journal of neuroscience.

[8]  Michael Häusser,et al.  Feed‐forward inhibition shapes the spike output of cerebellar Purkinje cells , 2005, The Journal of physiology.

[9]  Alex M Thomson,et al.  Presynaptic frequency filtering in the gamma frequency band; dual intracellular recordings in slices of adult rat and cat neocortex. , 2003, Cerebral cortex.

[10]  J. Buchanan Contributions of identifiable neurons and neuron classes to lamprey vertebrate neurobiology , 2001, Progress in Neurobiology.

[11]  Attila Losonczy,et al.  Cell type dependence and variability in the short‐term plasticity of EPSCs in identified mouse hippocampal interneurones , 2002, The Journal of physiology.

[12]  A. Lansner,et al.  The cortex as a central pattern generator , 2005, Nature Reviews Neuroscience.

[13]  S. Grillner,et al.  Calcium-dependent potassium channels play a critical role for burst termination in the locomotor network in lamprey. , 1994, Journal of neurophysiology.

[14]  R. Miles,et al.  Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea‐pig in vitro. , 1990, The Journal of physiology.

[15]  Alex M Thomson,et al.  Excitatory connections made by presynaptic cortico-cortical pyramidal cells in layer 6 of the neocortex. , 2005, Cerebral cortex.

[16]  S. Grillner,et al.  Fast and slow locomotor burst generation in the hemispinal cord of the lamprey. , 2003, Journal of neurophysiology.

[17]  F. Dudek,et al.  Dye-coupling between CA3 pyramidal cells in slices of rat hippocampus , 1980, Brain Research.

[18]  S. Grillner The motor infrastructure: from ion channels to neuronal networks , 2003, Nature Reviews Neuroscience.

[19]  B. Connors,et al.  Short-term dynamics of thalamocortical and intracortical synapses onto layer 6 neurons in neocortex. , 2002, Journal of neurophysiology.

[20]  Anders Lansner,et al.  Modeling of Substance P and 5-HT Induced Synaptic Plasticity in the Lamprey Spinal CPG: Consequences for Network Pattern Generation , 2001, Journal of Computational Neuroscience.

[21]  T. Freund,et al.  Differences between Somatic and Dendritic Inhibition in the Hippocampus , 1996, Neuron.

[22]  Erik De Schutter,et al.  Oscillations in the cerebellar cortex: a prediction of their frequency bands. , 2005, Progress in brain research.

[23]  G. Buzsáki,et al.  Interneurons of the hippocampus , 1998, Hippocampus.

[24]  E. G. Jones,et al.  Lamination and differential distribution of thalamic afferents within the sensory‐motor cortex of the squirrel monkey , 1975, The Journal of comparative neurology.

[25]  K. Martin,et al.  Intracortical excitation of spiny neurons in layer 4 of cat striate cortex in vitro. , 1999, Cerebral cortex.

[26]  E. White Cortical Circuits: Synaptic Organization of the Cerebral Cortex , 1989 .

[27]  V Taglietti,et al.  Theta-Frequency Bursting and Resonance in Cerebellar Granule Cells: Experimental Evidence and Modeling of a Slow K+-Dependent Mechanism , 2001, The Journal of Neuroscience.

[28]  H. Markram,et al.  Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat , 2004, The Journal of physiology.

[29]  Erik De Schutter,et al.  The Effect of NMDA Receptors on Gain Modulation , 2005, Neural Computation.

[30]  E De Schutter,et al.  Cerebellar Golgi cells in the rat: receptive fields and timing of responses to facial stimulation , 1999, The European journal of neuroscience.

[31]  D. Parker,et al.  Metaplastic Facilitation and Ultrastructural Changes in Synaptic Properties Are Associated with Long-Term Modulation of the Lamprey Locomotor Network , 2004, The Journal of Neuroscience.

[32]  Wade G. Regehr,et al.  Quantal events shape cerebellar interneuron firing , 2002, Nature Neuroscience.

[33]  O. Kiehn,et al.  Central Pattern Generators Deciphered by Molecular Genetics , 2004, Neuron.

[34]  S. Hestrin,et al.  Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex , 1998, Nature Neuroscience.

[35]  A. El Manira,et al.  Signaling Mechanisms of Metabotropic Glutamate Receptor 5 Subtype and Its Endogenous Role in a Locomotor Network , 2002, The Journal of Neuroscience.

[36]  S. Grillner,et al.  Identification of excitatory interneurons contributing to generation of locomotion in lamprey: structure, pharmacology, and function. , 1989, Journal of neurophysiology.

[37]  A. Thomson,et al.  Postsynaptic pyramidal target selection by descending layer III pyramidal axons: dual intracellular recordings and biocytin filling in slices of rat neocortex , 1998, Neuroscience.

[38]  R. Silver,et al.  Synaptic connections between layer 4 spiny neurone‐ layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column , 2002, The Journal of physiology.

[39]  B W Connors,et al.  Backward cortical projections to primary somatosensory cortex in rats extend long horizontal axons in layer I , 1998, The Journal of comparative neurology.

[40]  T. Kosaka,et al.  Gap Junctions Linking the Dendritic Network of GABAergic Interneurons in the Hippocampus , 2000, The Journal of Neuroscience.

[41]  N. Dale Excitatory synaptic drive for swimming mediated by amino acid receptors in the lamprey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  S. Grillner,et al.  Mechanisms of Rhythm Generation in a Spinal Locomotor Network Deprived of Crossed Connections: The Lamprey Hemicord , 2005, The Journal of Neuroscience.

[43]  I. Raman,et al.  Depression of Inhibitory Synaptic Transmission between Purkinje Cells and Neurons of the Cerebellar Nuclei , 2002, The Journal of Neuroscience.

[44]  Peter Somogyi,et al.  Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites , 1994, Nature.

[45]  N. Tamamaki,et al.  Hippocampal pyramidal cells excite inhibitory neurons through a single release site , 1993, Nature.

[46]  M. Castro-Alamancos,et al.  Short-term Plasticity in Thalamocortical Pathways: Cellular Mechanisms and Functional Roles , 1997, Reviews in the neurosciences.

[47]  S. Nakanishi Synaptic mechanisms of the cerebellar cortical network , 2005, Trends in Neurosciences.

[48]  A. Thomson,et al.  IPSPs elicited in CA1 pyramidal cells by putative basket cells in slices of adult rat hippocampus , 1999, The European journal of neuroscience.

[49]  Alex M Thomson,et al.  Layer 6 cortico-thalamic pyramidal cells preferentially innervate interneurons and generate facilitating EPSPs. , 2006, Cerebral cortex.

[50]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

[51]  G. Shepherd The Synaptic Organization of the Brain , 1979 .

[52]  Bert Sakmann,et al.  Monosynaptic Connections between Pairs of Spiny Stellate Cells in Layer 4 and Pyramidal Cells in Layer 5A Indicate That Lemniscal and Paralemniscal Afferent Pathways Converge in the Infragranular Somatosensory Cortex , 2005, The Journal of Neuroscience.

[53]  S. Grillner,et al.  Activity-Dependent Metaplasticity of Inhibitory and Excitatory Synaptic Transmission in the Lamprey Spinal Cord Locomotor Network , 1999, The Journal of Neuroscience.

[54]  Arnd Roth,et al.  Submillisecond AMPA Receptor-Mediated Signaling at a Principal Neuron–Interneuron Synapse , 1997, Neuron.

[55]  H. Markram,et al.  The neocortical microcircuit as a tabula rasa. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[56]  R Kötter,et al.  Morphology, electrophysiology and functional input connectivity of pyramidal neurons characterizes a genuine layer va in the primary somatosensory cortex. , 2006, Cerebral cortex.

[57]  Alan Peters,et al.  Cellular components of the cerebral cortex , 1984 .

[58]  N Dürmüller,et al.  Role of Thalamic and Cortical Neurons in Augmenting Responses and Self-Sustained Activity: Dual Intracellular Recordings In Vivo , 1998, The Journal of Neuroscience.

[59]  R. Traub,et al.  Axo-Axonal Coupling A Novel Mechanism for Ultrafast Neuronal Communication , 2001, Neuron.

[60]  Massimo Scanziani,et al.  Routing of spike series by dynamic circuits in the hippocampus , 2004, Nature.

[61]  S. Grillner,et al.  A new class of small inhibitory interneurones in the lamprey spinal cord , 1988, Brain Research.

[62]  S. Grillner,et al.  Presynaptic GABAA and GABAB Receptor‐mediated Phasic Modulation in Axons of Spinal Motor Interneurons , 1991, The European journal of neuroscience.

[63]  David Attwell,et al.  Tonic and Spillover Inhibition of Granule Cells Control Information Flow through Cerebellar Cortex , 2002, Neuron.

[64]  B Sakmann,et al.  AMPA Receptor Channels with Long-Lasting Desensitization in Bipolar Interneurons Contribute to Synaptic Depression in a Novel Feedback Circuit in Layer 2/3 of Rat Neocortex , 2001, The Journal of Neuroscience.

[65]  H. Markram,et al.  Synaptic dynamics control the timing of neuronal excitation in the activated neocortical microcircuit , 2004, The Journal of physiology.

[66]  S. Grillner,et al.  Newly identified 'glutamate interneurons' and their role in locomotion in the lamprey spinal cord. , 1987, Science.

[67]  C. Petersen,et al.  Short-term dynamics of synaptic transmission within the excitatory neuronal network of rat layer 4 barrel cortex. , 2002, Journal of neurophysiology.

[68]  A. Manira,et al.  Neuromodulation via Conditional Release of Endocannabinoids in the Spinal Locomotor Network , 2005, Neuron.

[69]  G Buzsáki,et al.  GABAergic Cells Are the Major Postsynaptic Targets of Mossy Fibers in the Rat Hippocampus , 1998, The Journal of Neuroscience.

[70]  Wade G. Regehr,et al.  Associative Short-Term Synaptic Plasticity Mediated by Endocannabinoids , 2005, Neuron.

[71]  D. Parker Activity-Dependent Feedforward Inhibition Modulates Synaptic Transmission in a Spinal Locomotor Network , 2003, The Journal of Neuroscience.

[72]  C. Hansel,et al.  Bidirectional Parallel Fiber Plasticity in the Cerebellum under Climbing Fiber Control , 2004, Neuron.

[73]  S. Hestrin,et al.  Electrical synapses define networks of neocortical GABAergic neurons , 2005, Trends in Neurosciences.

[74]  M. Häusser,et al.  Integration of quanta in cerebellar granule cells during sensory processing , 2004, Nature.

[75]  J. Bolz,et al.  Morphological types of projection neurons in layer 5 of cat visual cortex , 1990, The Journal of comparative neurology.

[76]  P. Somogyi,et al.  Defined types of cortical interneurone structure space and spike timing in the hippocampus , 2005, The Journal of physiology.

[77]  D. Linden,et al.  Long-Term Depression of the Cerebellar Climbing Fiber–Purkinje Neuron Synapse , 2000, Neuron.

[78]  Boris Barbour,et al.  Repetitive firing of rat cerebellar parallel fibres after a single stimulation , 2004, The Journal of physiology.

[79]  B. Barbour,et al.  Properties of Unitary Granule Cell→Purkinje Cell Synapses in Adult Rat Cerebellar Slices , 2002, The Journal of Neuroscience.

[80]  H. Markram A network of tufted layer 5 pyramidal neurons. , 1997, Cerebral cortex.

[81]  J. Deuchars,et al.  Large, deep layer pyramid-pyramid single axon EPSPs in slices of rat motor cortex display paired pulse and frequency-dependent depression, mediated presynaptically and self-facilitation, mediated postsynaptically. , 1993, Journal of neurophysiology.

[82]  R. W. Turner,et al.  Kv1 K+ Channels Control Purkinje Cell Output to Facilitate Postsynaptic Rebound Discharge in Deep Cerebellar Neurons , 2005, The Journal of Neuroscience.

[83]  John S. Barlow,et al.  The Cerebellum and Adaptive Control: Adaptive Control Models , 2002 .

[84]  S Grillner,et al.  The involvement of GABAB receptors and coupled G-proteins in spinal GABAergic presynaptic inhibition , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[85]  K. Sillar,et al.  Fast inhibitory synapses: targets for neuromodulation and development of vertebrate motor behaviour , 2002, Brain Research Reviews.

[86]  Urs Gerber,et al.  A frequency-dependent switch from inhibition to excitation in a hippocampal unitary circuit , 2004, Nature.

[87]  S. Grillner,et al.  Dual-component synaptic potentials in the lamprey mediated by excitatory amino acid receptors , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[88]  J. Deuchars,et al.  CA1 pyramidal to basket and bistratified cell EPSPs: dual intracellular recordings in rat hippocampal slices , 1998, The Journal of physiology.

[89]  D. Parker Variable Properties in a Single Class of Excitatory Spinal Synapse , 2003, The Journal of Neuroscience.

[90]  F. Edwards,et al.  Serotonin Drives a Novel GABAergic Synaptic Current Recorded in Rat Cerebellar Purkinje Cells: A Lugaro Cell to Purkinje Cell Synapse , 2003, The Journal of Neuroscience.

[91]  E. D’Angelo,et al.  Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum , 2001, Nature Neuroscience.

[92]  D. Kullmann,et al.  Tonically active GABAA receptors: modulating gain and maintaining the tone , 2004, Trends in Neurosciences.

[93]  A. Thomson,et al.  Facilitating pyramid to horizontal oriens‐alveus interneurone inputs: dual intracellular recordings in slices of rat hippocampus , 1998, The Journal of physiology.

[94]  A. Thomson,et al.  Interlaminar connections in the neocortex. , 2003, Cerebral cortex.

[95]  H. Markram,et al.  t Synchrony Generation in Recurrent Networks with Frequency-Dependent Synapses , 2000, The Journal of Neuroscience.

[96]  Miles A Whittington,et al.  Cellular mechanisms of neuronal population oscillations in the hippocampus in vitro. , 2004, Annual review of neuroscience.

[97]  C. McBain,et al.  Interneuron Diversity series: Containing the detonation – feedforward inhibition in the CA3 hippocampus , 2003, Trends in Neurosciences.

[98]  T. McNamara,et al.  Cognitive maps and the hippocampus , 2003, Trends in Cognitive Sciences.

[99]  A. Thomson,et al.  Differential sensitivity to Zolpidem of IPSPs activated by morphologically identified CA1 interneurons in slices of rat hippocampus , 2000, The European journal of neuroscience.

[100]  P. Somogyi,et al.  The hippocampal CA3 network: An in vivo intracellular labeling study , 1994, The Journal of comparative neurology.

[101]  Yun Wang,et al.  Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2-5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro. , 2002, Cerebral cortex.

[102]  Ranulfo Romo,et al.  Presynaptic inhibition and neural control , 1998 .

[103]  D. Henze,et al.  The multifarious hippocampal mossy fiber pathway: a review , 2000, Neuroscience.

[104]  H. Markram,et al.  Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. , 2000, Science.

[105]  R. Llinás The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. , 1988, Science.