Striatal cellular properties conserved from lampreys to mammals

Non‐technical summary  The striatum is a structure in the forebrain that plays an important role in the control of movements. Diseases that affect this region lead to severe movement disorders, such as Parkinson's disease. We show here in the lamprey, the oldest vertebrate group to emerge, that the characteristic cellular properties of neurons in striatum in many respects are similar to those of mammals. Our results show how specific ion channels, including particular potassium channels (Kir) that are open at very negative membrane potentials help shape the way these cells respond to and transmit neuronal signals. These specific features are thus conserved throughout vertebrate evolution, and contribute thereby to our understanding of the mode of operation of striatum, at a cellular level, and how movements are controlled.

[1]  D. Surmeier,et al.  Kv1.2-containing K+ channels regulate subthreshold excitability of striatal medium spiny neurons. , 2004, Journal of neurophysiology.

[2]  S. Grillner,et al.  Sodium‐dependent potassium channels of a Slack‐like subtype contribute to the slow afterhyperpolarization in lamprey spinal neurons , 2007, The Journal of physiology.

[3]  Menek Goldstein,et al.  Neurotensin‐like Peptides in the CNS of Lampreys: Chromatographic Characterization and Immunohistochemical Localization with Reference to Aminergic Markers , 1990, The European journal of neuroscience.

[4]  S. Grillner,et al.  Distribution of histaminergic neurons in the brain of the lamprey lampetra fluviatilis as revealed by histamine‐immunohistochemistry , 1990, The Journal of comparative neurology.

[5]  C. Wilson,et al.  Intracellular recording of identified neostriatal patch and matrix spiny cells in a slice preparation preserving cortical inputs. , 1989, Journal of neurophysiology.

[6]  Sten Grillner,et al.  Descending GABAergic projections to the mesencephalic locomotor region in the lamprey Petromyzon marinus , 2007, The Journal of comparative neurology.

[7]  S. Grillner,et al.  Forebrain dopamine depletion impairs motor behavior in lamprey , 2008, The European journal of neuroscience.

[8]  Occurrence and distribution of substance P-related immunoreactivity in the brain of adult lampreys, Petromyzon marinus and Entosphenus tridentatus. , 1986, General and comparative endocrinology.

[9]  C. Wilson,et al.  Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  Charles J. Wilson,et al.  Membrane potential synchrony of simultaneously recorded striatal spiny neurons in vivo , 1998, Nature.

[11]  M. Farries,et al.  Electrophysiological properties of avian basal ganglia neurons recorded in vitro. , 2000, Journal of neurophysiology.

[12]  R. Northcutt,et al.  Afferent and efferent connections of the lateral and medial pallia of the silver lamprey. , 1997, Brain, behavior and evolution.

[13]  Charles J. Wilson,et al.  GABAergic microcircuits in the neostriatum , 2004, Trends in Neurosciences.

[14]  O. Marín,et al.  Distribution of choline acetyltransferase‐immunoreactive structures in the lamprey brain , 2001, The Journal of comparative neurology.

[15]  Y. Kawaguchi,et al.  Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  A. El Manira,et al.  Characterization of a high-voltage-activated IA current with a role in spike timing and locomotor pattern generation , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[17]  S. Grillner,et al.  GABA distribution in lamprey is phylogenetically conserved , 2007, The Journal of comparative neurology.

[18]  N. Standen,et al.  A potential‐ and time‐dependent blockade of inward rectification in frog skeletal muscle fibres by barium and strontium ions. , 1978, The Journal of physiology.

[19]  Charles J. Wilson,et al.  The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  A. Sadikot,et al.  Neurogenesis and stereological morphometry of calretinin‐immunoreactive GABAergic interneurons of the neostriatum , 2004, The Journal of comparative neurology.

[21]  S. Grillner,et al.  Diencephalic locomotor region in the lamprey--afferents and efferent control. , 2008, Journal of neurophysiology.

[22]  S. Grillner,et al.  Mechanisms for selection of basic motor programs – roles for the striatum and pallidum , 2005, Trends in Neurosciences.

[23]  P. Redgrave,et al.  What is reinforced by phasic dopamine signals? , 2008, Brain Research Reviews.

[24]  T. Hökfelt,et al.  Cholecystokinin and Cultured Spinal Neurons Immunohistochemistry, Receptor Binding, and Neurophysiology a , 1985, Annals of the New York Academy of Sciences.

[25]  S. Grillner,et al.  Evolutionary Conservation of the Basal Ganglia as a Common Vertebrate Mechanism for Action Selection , 2011, Current Biology.

[26]  Max Kleiman-Weiner,et al.  Differential electrophysiological properties of dopamine D1 and D2 receptor‐containing striatal medium‐sized spiny neurons , 2008, The European journal of neuroscience.

[27]  D. Surmeier,et al.  Cholinergic modulation of Kir2 channels selectively elevates dendritic excitability in striatopallidal neurons , 2007, Nature Neuroscience.

[28]  A. Constanti,et al.  Mechanism of block by ZD 7288 of the hyperpolarization-activated inward rectifying current in guinea pig substantia nigra neurons in vitro. , 1995, Journal of neurophysiology.

[29]  Alessandro Stefani,et al.  Developmental regulation of a slowly-inactivating potassium conductance in rat neostriatal neurons , 1991, Neuroscience Letters.

[30]  R. Dubuc,et al.  Immunohistochemical distribution of tachykinins in the CNS of the lamprey Petromyzon marinus , 2004, The Journal of comparative neurology.

[31]  S. Grillner,et al.  Neural bases of goal-directed locomotion in vertebrates—An overview , 2008, Brain Research Reviews.

[32]  J. Bargas,et al.  Dopaminergic Modulation of Spiny Neurons in the Turtle Striatum , 2010, Cellular and Molecular Neurobiology.

[33]  J. Tepper,et al.  Basal ganglia macrocircuits. , 2007, Progress in brain research.

[34]  M. Pombal,et al.  Distribution of galanin‐like immunoreactive elements in the brain of the adult lamprey Lampetra fluviatilis , 1996, The Journal of comparative neurology.

[35]  D. Surmeier,et al.  D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons , 2007, Trends in Neurosciences.

[36]  Sten Grillner,et al.  Organization of the lamprey striatum – transmitters and projections , 1997, Brain Research.

[37]  M. Wikström,et al.  A lamprey striatal brain slice preparation for patch-clamp recordings , 2007, Journal of Neuroscience Methods.

[38]  S. Grillner,et al.  Role of apamin-sensitive k(ca) channels for reticulospinal synaptic transmission to motoneuron and for the afterhyperpolarization. , 2002, Journal of neurophysiology.

[39]  J. Tepper,et al.  Functional diversity and specificity of neostriatal interneurons , 2004, Current Opinion in Neurobiology.

[40]  R. North,et al.  Inward rectification in rat nucleus accumbens neurons. , 1989, Journal of neurophysiology.

[41]  Sten Grillner,et al.  Afferents of the lamprey striatum with special reference to the dopaminergic system: A combined tracing and immunohistochemical study , 1997, The Journal of comparative neurology.

[42]  R. North,et al.  Membrane properties and synaptic responses of rat striatal neurones in vitro. , 1991, The Journal of physiology.