Nitric oxide-dependent long-term depression but not endocannabinoid-mediated long-term potentiation is crucial for visual recognition memory

•  Perirhinal cortex (Prh) is critically involved in visual recognition memory and synaptic plasticity. •  Nitric oxide and endocannabinoids (eCBs) have been shown to act as retrograde messengers in synaptic plasticity in several brain areas, but no study has yet investigated their role in synaptic plasticity in Prh. •  Evidence is still lacking of a retrograde messenger involved in synaptic plasticity in Prh. •  In this study, we show that NO is involved in long‐term depression (LTD) but not in long‐term potentiation (LTP). Conversely, eCBs are involved in LTP but not in LTD. Crucially, inhibiition of NO signalling prevents visual recognition memory acquisition, whilst inhibition of eCB signalling does not affect recognition memory. •  These results suggest that LTD but not LTP is a neuronal correlate of visual recognition memory.

[1]  A. Blokland,et al.  Rolipram reverses scopolamine-induced and time-dependent memory deficits in object recognition by different mechanisms of action , 2006, Neurobiology of Learning and Memory.

[2]  Malcolm W. Brown,et al.  Recognition memory: Material, processes, and substrates , 2010, Hippocampus.

[3]  K. Hsu,et al.  Activation of muscarinic acetylcholine receptors induces a nitric oxide-dependent long-term depression in rat medial prefrontal cortex. , 2010, Cerebral cortex.

[4]  Pedro Grandes,et al.  Molecular Components and Functions of the Endocannabinoid System in Mouse Prefrontal Cortex , 2007, PloS one.

[5]  Mohamed T. Ghorbel,et al.  Expression of Long-Term Depression Underlies Visual Recognition Memory , 2008, Neuron.

[6]  E. Kandel,et al.  Nitric Oxide Acts Directly in the Presynaptic Neuron to Produce Long-Term Potentiationin Cultured Hippocampal Neurons , 1996, Cell.

[7]  R. Hawkins,et al.  Presynaptic Role of cGMP-Dependent Protein Kinase during Long-Lasting Potentiation , 2001, The Journal of Neuroscience.

[8]  A. Blokland,et al.  Effects of two selective phosphodiesterase type 5 inhibitors, sildenafil and vardenafil, on object recognition memory and hippocampal cyclic GMP levels in the rat , 2002, Neuroscience.

[9]  J Garthwaite,et al.  Nitric oxide signaling in the central nervous system. , 1995, Annual review of physiology.

[10]  J. Delacour,et al.  A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data , 1988, Behavioural Brain Research.

[11]  I. Akirav,et al.  Cannabinoids modulate hippocampal memory and plasticity , 2009, Hippocampus.

[12]  H. Haas,et al.  Long‐term depression of cortico‐striatal synaptic transmission by DHPG depends on endocannabinoid release and nitric oxide synthesis , 2007, The European journal of neuroscience.

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

[14]  W. Zieglgänsberger,et al.  The endogenous cannabinoid system controls extinction of aversive memories , 2002, Nature.

[15]  Spartaco Santi,et al.  Induction of long-term potentiation and depression is reflected by corresponding changes in secretion of endogenous brain-derived neurotrophic factor. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[16]  John Garthwaite,et al.  On the Role of Nitric Oxide in Hippocampal Long-Term Potentiation , 2003, The Journal of Neuroscience.

[17]  G. Collingridge,et al.  Differential Roles of NR2A and NR2B-Containing NMDA Receptors in Cortical Long-Term Potentiation and Long-Term Depression , 2004, The Journal of Neuroscience.

[18]  Graham L. Collingridge,et al.  Capabilities of the WinLTP data acquisition program extending beyond basic LTP experimental functions , 2007, Journal of Neuroscience Methods.

[19]  N. Pitsikas,et al.  Effects of the nitric oxide synthase inhibitor L-NAME on different memory components as assessed in the object recognition task in the rat , 2010, Behavioural Brain Research.

[20]  J. Steinmetz,et al.  A nitric oxide synthase inhibitor delays the formation of learning-related neural activity in the cerebellar interpositus nucleus during rabbit eyelid conditioning , 1996, Pharmacology Biochemistry and Behavior.

[21]  K. Mackie,et al.  Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system , 1998, Neuroscience.

[22]  D. Bilkey.  Long-term potentiation in the in vitro perirhinal cortex displays associative properties , 1996, Brain Research.

[23]  S. Nagao,et al.  Acute effects of tetrahydrobiopterin on the dynamic characteristics and adaptability of vestibulo-ocular reflex in normal and flocculus lesioned rabbits , 1997, Neuroscience Letters.

[24]  L. Swanson.  The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[25]  P. Stanton,et al.  NMDA-Dependent, But Not Group I Metabotropic Glutamate Receptor-Dependent, Long-Term Depression at Schaffer Collateral–CA1 Synapses Is Associated with Long-Term Reduction of Release from the Rapidly Recycling Presynaptic Vesicle Pool , 2006, The Journal of Neuroscience.

[26]  J. Garthwaite,et al.  On the selectivity of neuronal NOS inhibitors , 2013, British journal of pharmacology.

[27]  G. Böhme,et al.  Altered synaptic plasticity and memory formation in nitric oxide synthase inhibitor-treated rats. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[28]  E. Kandel,et al.  Presynaptic and Postsynaptic Roles of NO, cGK, and RhoA in Long-Lasting Potentiation and Aggregation of Synaptic Proteins , 2005, Neuron.

[29]  A. Ennaceur,et al.  A new one-trial test for neurobiological studies of memory in rats. III. Spatial vs. non-spatial working memory , 1992, Behavioural Brain Research.

[30]  P. Castillo,et al.  Endocannabinoid signaling and long-term synaptic plasticity. , 2009, Annual review of physiology.

[31]  I. Forsythe,et al.  Nitric Oxide Signaling in Brain Function, Dysfunction, and Dementia , 2010, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[32]  B. Cravatt,et al.  Inhibition of Fatty-Acid Amide Hydrolase Accelerates Acquisition and Extinction Rates in a Spatial Memory Task , 2007, Neuropsychopharmacology.

[33]  John P. Aggleton,et al.  cAMP Responsive Element-Binding Protein Phosphorylation Is Necessary for Perirhinal Long-Term Potentiation and Recognition Memory , 2005, The Journal of Neuroscience.

[34]  Z. Bashir,et al.  Activation of muscarinic receptors induces protein synthesis‐dependent long‐lasting depression in the perirhinal cortex , 2001, The European journal of neuroscience.

[35]  T. Tsumoto,et al.  Regulation of excitability and plasticity by endocannabinoids and PKA in developing hippocampus , 2008, Proceedings of the National Academy of Sciences.

[36]  E. Kandel,et al.  Activity-dependent long-term enhancement of transmitter release by presynaptic 3′,5′-cyclic GMP in cultured hippocampal neurons , 1995, Nature.

[37]  D. Bilkey,et al.  Nitric oxide synthase and arginase in the rat hippocampus and the entorhinal, perirhinal, postrhinal, and temporal cortices: Regional variations and age‐related changes , 2003, Hippocampus.

[38]  G. Collingridge,et al.  Metabotropic Glutamate Receptor-Mediated LTD Involves Two Interacting Ca2+ Sensors, NCS-1 and PICK1 , 2008, Neuron.

[39]  U. Eysel,et al.  Long-Term Potentiation in the Visual Cortex Requires Both Nitric Oxide Receptor Guanylyl Cyclases , 2007, The Journal of Neuroscience.

[40]  Malcolm W. Brown,et al.  Recognition memory: What are the roles of the perirhinal cortex and hippocampus? , 2001, Nature Reviews Neuroscience.

[41]  David Robbe,et al.  Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[42]  M. Parmentier,et al.  Enhancement of memory in cannabinoid CB1 receptor knock-out mice. , 1999, European journal of pharmacology.

[43]  Z. Bashir,et al.  Learning-Specific Changes in Long-Term Depression in Adult Perirhinal Cortex , 2008, The Journal of Neuroscience.

[44]  Z. Bashir,et al.  L-Type Voltage-Dependent Calcium Channel Antagonists Impair Perirhinal Long-Term Recognition Memory and Plasticity Processes , 2009, The Journal of Neuroscience.

[45]  J. Garthwaite,et al.  Exogenous nitric oxide causes potentiation of hippocampal synaptic transmission during low‐frequency stimulation via the endogenous nitric oxide–cGMP pathway , 2001, The European journal of neuroscience.

[46]  A. Ennaceur,et al.  Effects of lesions of the Substantia Innominata/Ventral Pallidum, globus pallidus and medial septum on rat's performance in object-recognition and radial-maze tasks: physostigmine and amphetamine treatments. , 1998, Pharmacological research.

[47]  A. Egerton,et al.  Cannabinoids and prefrontal cortical function: Insights from preclinical studies , 2006, Neuroscience & Biobehavioral Reviews.

[48]  J. Garthwaite.  Concepts of neural nitric oxide-mediated transmission , 2008, The European journal of neuroscience.

[49]  R. Malenka,et al.  Postsynaptic TRPV1 triggers cell type–specific long-term depression in the nucleus accumbens , 2010, Nature Neuroscience.

[50]  Toshihide Tabata,et al.  Type-1 metabotropic glutamate receptor in cerebellar Purkinje cells: a key molecule responsible for long-term depression, endocannabinoid signalling and synapse elimination , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[51]  M. W. Brown,et al.  Input- and layer-dependent synaptic plasticity in the rat perirhinal cortex in vitro , 1999, Neuroscience.

[52]  G. Riedel,et al.  Cannabinoid function in learning, memory and plasticity. , 2005, Handbook of experimental pharmacology.

[53]  A. Araque,et al.  Endocannabinoids Potentiate Synaptic Transmission through Stimulation of Astrocytes , 2010, Neuron.

[54]  J. Aggleton,et al.  The Different Effects on Recognition Memory of Perirhinal Kainate and NMDA Glutamate Receptor Antagonism: Implications for Underlying Plasticity Mechanisms , 2006, The Journal of Neuroscience.

[55]  Malcolm W. Brown,et al.  Cholinergic Neurotransmission Is Essential for Perirhinal Cortical Plasticity and Recognition Memory , 2003, Neuron.

[56]  Z. Bashir,et al.  Experience-dependent modification of mechanisms of long-term depression , 2006, Nature Neuroscience.

[57]  M. Marletta,et al.  Potent and selective inhibition of neuronal nitric oxide synthase by N(ω)-propyl-L-arginine , 1997 .

[58]  Z. Bashir,et al.  A temporally distinct role for group I and group II metabotropic glutamate receptors in object recognition memory. , 2006, Learning & memory.

[59]  M. Parmentier,et al.  Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. , 1999, Science.

[60]  Allan R. Jones,et al.  Genome-wide atlas of gene expression in the adult mouse brain , 2007, Nature.

[61]  Jung Hoon Shin,et al.  An NMDA receptor/nitric oxide cascade is involved in cerebellar LTD but is not localized to the parallel fiber terminal. , 2005, Journal of neurophysiology.

[62]  G. Barker,et al.  Recognition Memory for Objects, Place, and Temporal Order: A Disconnection Analysis of the Role of the Medial Prefrontal Cortex and Perirhinal Cortex , 2007, The Journal of Neuroscience.

[63]  B. Lutz.  The Endocannabinoid System and Extinction Learning , 2007, Molecular Neurobiology.

[64]  Sophie L. Dix,et al.  Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition , 1999, Behavioural Brain Research.

[65]  D. Bilkey,et al.  Cannabinoid CB1 receptor protein expression in the rat hippocampus and entorhinal, perirhinal, postrhinal and temporal cortices: regional variations and age-related changes , 2003, Brain Research.

[66]  M. Cassell,et al.  Perirhinal cortex projections to the amygdaloid complex and hippocampal formation in the rat , 1999, The Journal of comparative neurology.

[67]  P. Stanton,et al.  Induction of hippocampal LTD requires nitric-oxide-stimulated PKG activity and Ca2+ release from cyclic ADP-ribose-sensitive stores. , 1999, Journal of neurophysiology.