Tuning the network: modulation of neuronal microcircuits in the spinal cord and hippocampus

Adaptation of an organism to its changing environment ultimately depends on the modification of neuronal activity. The dynamic interaction between cellular components within neuronal networks relies on fast synaptic interaction via ionotropic receptors. However, neuronal networks are also subject to modulation mediated by various metabotropic G-protein-coupled receptors that modify synaptic and neuronal function. Modulation increases the functional complexity of a network, because the same cellular components can produce different outputs depending on the behavioural state of the animal. This review, which is part of the TINS Microcircuits Special Feature, provides an overview of neuromodulation in two neuronal circuits that both produce oscillatory activity but differ fundamentally in function. Hippocampal circuits are compared with the spinal networks generating locomotion, with a view to exploring common principles of neuromodulatory activity.

[1]  D. Parker,et al.  Presynaptic and interactive peptidergic modulation of reticulospinal synaptic inputs in the lamprey. , 2000, Journal of neurophysiology.

[2]  S. Grillner,et al.  The spinal GABA system modulates burst frequency and intersegmental coordination in the lamprey: differential effects of GABAA and GABAB receptors. , 1993, Journal of neurophysiology.

[3]  Hannah Monyer,et al.  Differential involvement of oriens/pyramidale interneurones in hippocampal network oscillations in vitro , 2005, The Journal of physiology.

[4]  M. Scanziani GABA Spillover Activates Postsynaptic GABAB Receptors to Control Rhythmic Hippocampal Activity , 2000, Neuron.

[5]  Sten Grillner,et al.  Control of lamprey locomotor neurons by colocalized monoamine transmitters , 1995, Nature.

[6]  M. Frotscher,et al.  Subcellular Localization of Metabotropic GABAB Receptor Subunits GABAB1a/b and GABAB2 in the Rat Hippocampus , 2003, The Journal of Neuroscience.

[7]  Uwe Heinemann,et al.  Dopamine depresses cholinergic oscillatory network activity in rat hippocampus , 2003, The European journal of neuroscience.

[8]  H. Monyer,et al.  Differential Expression of Group I Metabotropic Glutamate Receptors in Functionally Distinct Hippocampal Interneurons , 2000, The Journal of Neuroscience.

[9]  S. J. Martin Activation of metabotropic glutamate receptors induces gamma frequency oscillations in the rat dentate gyrus in vivo , 2001, Neuropharmacology.

[10]  A. El Manira,et al.  Interaction between Metabotropic and Ionotropic Glutamate Receptors Regulates Neuronal Network Activity , 2000, The Journal of Neuroscience.

[11]  Trevor Sharp,et al.  A review of central 5-HT receptors and their function , 1999, Neuropharmacology.

[12]  Jeremy K. Seamans,et al.  Corrigendum to “The principal features and mechanisms of dopamine modulation in the prefrontal cortex” [Prog. Neurobiol. 74 (2004) 1–58] , 2004, Progress in Neurobiology.

[13]  O. Paulsen,et al.  Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro , 1998, Nature.

[14]  C. McBain,et al.  Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  S Grillner,et al.  Activation of pharmacologically distinct metabotropic glutamate receptors depresses reticulospinal-evoked monosynaptic EPSPs in the lamprey spinal cord. , 1996, Journal of neurophysiology.

[16]  B. Jacobs,et al.  Serotonin and motor activity , 1997, Current Opinion in Neurobiology.

[17]  C. Harley,et al.  Locus Ceruleus Activation Suppresses Feedforward Interneurons and Reduces β-γ Electroencephalogram Frequencies While It Enhances θ Frequencies in Rat Dentate Gyrus , 2005, The Journal of Neuroscience.

[18]  T. Freund,et al.  Role of endogenous cannabinoids in synaptic signaling. , 2003, Physiological reviews.

[19]  J. Seamans,et al.  The principal features and mechanisms of dopamine modulation in the prefrontal cortex , 2004, Progress in Neurobiology.

[20]  R. Traub,et al.  Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation , 1995, Nature.

[21]  G. Buzsáki Theta Oscillations in the Hippocampus , 2002, Neuron.

[22]  E Marder,et al.  Modulators with Convergent Cellular Actions Elicit Distinct Circuit Outputs , 2001, The Journal of Neuroscience.

[23]  S. Grillner,et al.  Locomotor‐Related Presynaptic Modulation of Primary Afferents in the Lamprey , 1997, The European journal of neuroscience.

[24]  R. Nicoll,et al.  Endocannabinoid Signaling in the Brain , 2002, Science.

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

[26]  C. Berridge,et al.  The locus coeruleus–noradrenergic system: modulation of behavioral state and state-dependent cognitive processes , 2003, Brain Research Reviews.

[27]  B. Alger,et al.  Metabotropic Glutamate Receptors Drive the Endocannabinoid System in Hippocampus , 2001, The Journal of Neuroscience.

[28]  R. Miles,et al.  How Many Subtypes of Inhibitory Cells in the Hippocampus? , 1998, Neuron.

[29]  M. Hajós,et al.  Regulation of Septo-Hippocampal Activity by 5-Hydroxytryptamine2C Receptors , 2003, Journal of Pharmacology and Experimental Therapeutics.

[30]  Ayae Kinoshita,et al.  Differential Presynaptic Localization of Metabotropic Glutamate Receptor Subtypes in the Rat Hippocampus , 1997, The Journal of Neuroscience.

[31]  P. Goldman-Rakic,et al.  Localization of dopamine D4 receptors in GABAergic neurons of the primate brain , 1996, Nature.

[32]  S. Baraban,et al.  Interneuron Diversity series: Interneuronal neuropeptides – endogenous regulators of neuronal excitability , 2004, Trends in Neurosciences.

[33]  Fiona E. N. LeBeau,et al.  A Model of Atropine‐Resistant Theta Oscillations in Rat Hippocampal Area CA1 , 2002, The Journal of physiology.

[34]  S. Grillner,et al.  Low-voltage-activated calcium channels in the lamprey locomotor network: simulation and experiment. , 1997, Journal of neurophysiology.

[35]  A. El Manira,et al.  mGluR1, but not mGluR5, mediates depolarization of spinal cord neurons by blocking a leak current. , 2003, Journal of neurophysiology.

[36]  P. Saggau,et al.  Inhibition of Synaptic Transmission by Neuropeptide Y in Rat Hippocampal Area CA1: Modulation of Presynaptic Ca2+Entry , 1997, The Journal of Neuroscience.

[37]  R. Perrins,et al.  Cholinergic contribution to excitation in a spinal locomotor central pattern generator in Xenopus embryos. , 1995, Journal of neurophysiology.

[38]  J. Kaas,et al.  The evolution of the neocortex in mammals: how is phenotypic diversity generated? , 2005, Current Opinion in Neurobiology.

[39]  Juan Lerma,et al.  Roles and rules of kainate receptors in synaptic transmission , 2003, Nature Reviews Neuroscience.

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

[41]  C. Davies,et al.  Cholinergic modulation of hippocampal cells and circuits , 2005, The Journal of physiology.

[42]  M. Raiteri,et al.  International Union of Pharmacology. XXXIII. Mammalian γ-Aminobutyric AcidB Receptors: Structure and Function , 2002, Pharmacological Reviews.

[43]  C. Harley,et al.  Locus ceruleus activation suppresses feedforward interneurons and reduces beta-gamma electroencephalogram frequencies while it enhances theta frequencies in rat dentate gyrus. , 2005, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  J. Buchanan,et al.  Cholinergic modulation of the locomotor network in the lamprey spinal cord. , 2004, Journal of neurophysiology.

[45]  L. Acsády,et al.  Serotonergic control of the hippocampus via local inhibitory interneurons. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[46]  P. Somogyi,et al.  Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo , 2004, Nature Neuroscience.

[47]  Peter Somogyi,et al.  Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro , 2000, The Journal of physiology.

[48]  S Grillner,et al.  GABAB receptor activation causes a depression of low- and high-voltage-activated Ca2+ currents, postinhibitory rebound, and postspike afterhyperpolarization in lamprey neurons. , 1993, Journal of neurophysiology.

[49]  R. S. Sloviter,et al.  Localization of GABAB (R1) receptors in the rat hippocampus by immunocytochemistry and high resolution autoradiography, with specific reference to its localization in identified hippocampal interneuron subpopulations , 1999, Neuropharmacology.

[50]  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.

[51]  S Grillner,et al.  Interactive effects of the GABABergic modulation of calcium channels and calcium-dependent potassium channels in lamprey. , 1999, Journal of neurophysiology.

[52]  B. Alger Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids , 2002, Progress in Neurobiology.

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

[54]  D. Zenisek,et al.  Recent progress towards understanding the synaptic ribbon , 2005, Current Opinion in Neurobiology.

[55]  Anders Lansner,et al.  Computer simulation of the segmental neural network generating locomotion in lamprey by using populations of network interneurons , 2004, Biological Cybernetics.

[56]  J. Wess,et al.  Muscarinic Induction of Hippocampal Gamma Oscillations Requires Coupling of the M1 Receptor to Two Mixed Cation Currents , 2002, Neuron.

[57]  J. Lacaille,et al.  A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[58]  A. Levey,et al.  Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[59]  J. Lisman,et al.  Contribution of Ih and GABAB to synaptically induced afterhyperpolarizations in CA1: a brake on the NMDA response. , 2004, Journal of neurophysiology.

[60]  S Grillner,et al.  Neuronal mechanisms of synaptic and network plasticity in the lamprey spinal cord. , 2000, Progress in brain research.

[61]  P. Somogyi,et al.  Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo , 2003, Nature.

[62]  B. Alger,et al.  Postsynaptic spike firing reduces synaptic GABAA responses in hippocampal pyramidal cells , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[63]  V. Doze,et al.  Excitatory actions of norepinephrine on multiple classes of hippocampal CA1 interneurons , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[64]  R. Anwyl Metabotropic glutamate receptors: electrophysiological properties and role in plasticity , 1999, Brain Research Reviews.

[65]  Sten Grillner,et al.  Co‐localized neuropeptide Y and GABA have complementary presynaptic effects on sensory synaptic transmission , 1998, The European journal of neuroscience.

[66]  K. Yau,et al.  Non-image-forming ocular photoreception in vertebrates , 2005, Current Opinion in Neurobiology.

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

[68]  S. Grillner,et al.  Inhibition of N- and L-type Ca2+ currents by dopamine in lamprey spinal motoneurons. , 1999, Neuroreport.

[69]  C. Chapman,et al.  Cholinergic Induction of Theta-Frequency Oscillations in Hippocampal Inhibitory Interneurons and Pacing of Pyramidal Cell Firing , 1999, The Journal of Neuroscience.

[70]  O. Paulsen,et al.  Spike Timing of Distinct Types of GABAergic Interneuron during Hippocampal Gamma Oscillations In Vitro , 2004, The Journal of Neuroscience.

[71]  A. Manira,et al.  Group III mGluR-mediated depression of sensory synaptic transmission , 2002, Brain Research.

[72]  S. Grillner,et al.  The spinal GABAergic system is a strong modulator of burst frequency in the lamprey locomotor network. , 2004, Journal of neurophysiology.

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

[74]  S. Grillner,et al.  5‐HT inhibits N‐type but not L‐type Ca2+ channels via 5‐HT1A receptors in lamprey spinal neurons , 2003, The European journal of neuroscience.

[75]  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.

[76]  Q. Gu,et al.  Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity , 2002, Neuroscience.

[77]  S. Grillner,et al.  The spinal 5-HT system contributes to the generation of fictive locomotion in lamprey , 2000, Brain Research.

[78]  S. Grillner,et al.  Ion channels of importance for the locomotor pattern generation in the lamprey brainstem‐spinal cord , 2001, The Journal of physiology.

[79]  O. Paulsen,et al.  Distinct properties of carbachol- and DHPG-induced network oscillations in hippocampal slices , 2004, Neuropharmacology.

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

[81]  Ken Mackie,et al.  Presynaptically Located CB1 Cannabinoid Receptors Regulate GABA Release from Axon Terminals of Specific Hippocampal Interneurons , 1999, The Journal of Neuroscience.

[82]  A. Fisahn,et al.  Kainate receptors and rhythmic activity in neuronal networks: hippocampal gamma oscillations as a tool , 2005, The Journal of physiology.

[83]  I. Tracey Nociceptive processing in the human brain , 2005, Current Opinion in Neurobiology.

[84]  R Lujan,et al.  Perisynaptic Location of Metabotropic Glutamate Receptors mGluR1 and mGluR5 on Dendrites and Dendritic Spines in the Rat Hippocampus , 1996, The European journal of neuroscience.

[85]  E. Lumpkin,et al.  Feeling the pressure in mammalian somatosensation , 2005, Current Opinion in Neurobiology.

[86]  Attila Losonczy,et al.  Persistently active cannabinoid receptors mute a subpopulation of hippocampal interneurons. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[87]  K. Roche,et al.  mGluR7 Is a Metaplastic Switch Controlling Bidirectional Plasticity of Feedforward Inhibition , 2005, Neuron.

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

[89]  Howard V. Wheal,et al.  Metabotropic-Mediated Kainate Receptor Regulation of IsAHP and Excitability in Pyramidal Cells , 2002, Neuron.

[90]  T. Jay Dopamine: a potential substrate for synaptic plasticity and memory mechanisms , 2003, Progress in Neurobiology.