Associative Hebbian Synaptic Plasticity in Primate Visual Cortex

In primates, the functional connectivity of adult primary visual cortex is susceptible to be modified by sensory training during perceptual learning. It is widely held that this type of neural plasticity might involve mechanisms like long-term potentiation (LTP) and long-term depression (LTD). NMDAR-dependent forms of LTP and LTD are particularly attractive because in rodents they can be induced in a Hebbian manner by near coincidental presynaptic and postsynaptic firing, in a paradigm termed spike timing-dependent plasticity (STDP). These fundamental properties of LTP and LTD, Hebbian induction and NMDAR dependence, have not been examined in primate cortex. Here we demonstrate these properties in the primary visual cortex of the rhesus macaque (Macaca mulatta), and also show that, like in rodents, STDP is gated by neuromodulators. These findings indicate that the cellular principles governing cortical plasticity are conserved across mammalian species, further validating the use of rodents as a model system.

[1]  SM Dudek,et al.  Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  G. Shepherd,et al.  Long-term modifications of synaptic efficacy in the human inferior and middle temporal cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[3]  N W Daw,et al.  Critical periods and amblyopia. , 1998, Archives of ophthalmology.

[4]  M. Bear,et al.  Modulation of Long-Term Synaptic Depression in Visual Cortex by Acetylcholine and Norepinephrine , 1999, The Journal of Neuroscience.

[5]  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.

[6]  Z. J. Huang,et al.  Maturation of GABAergic transmission and the timing of plasticity in visual cortex , 2005, Brain Research Reviews.

[7]  N. Spruston,et al.  Postsynaptic depolarization requirements for LTP and LTD: a critique of spike timing-dependent plasticity , 2005, Nature Neuroscience.

[8]  A. Kirkwood,et al.  Cross-modal regulation of synaptic AMPA receptors in primary sensory cortices by visual experience , 2006, Nature Neuroscience.

[9]  Mario Treviño,et al.  Sequential Development of Long-Term Potentiation and Depression in Different Layers of the Mouse Visual Cortex , 2007, The Journal of Neuroscience.

[10]  A. Kirkwood,et al.  Neuromodulators Control the Polarity of Spike-Timing-Dependent Synaptic Plasticity , 2007, Neuron.

[11]  K. Fox,et al.  Sensory Deprivation Unmasks a PKA-Dependent Synaptic Plasticity Mechanism that Operates in Parallel with CaMKII , 2008, Neuron.

[12]  M. Bear,et al.  Bidirectional synaptic mechanisms of ocular dominance plasticity in visual cortex , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[13]  Y. Dan,et al.  Spike timing-dependent plasticity: a Hebbian learning rule. , 2008, Annual review of neuroscience.

[14]  L. McMahon,et al.  Layer 2/3 synapses in monocular and binocular regions of tree shrew visual cortex express mAChR-dependent long-term depression and long-term potentiation. , 2008, Journal of neurophysiology.

[15]  D. Feldman Synaptic mechanisms for plasticity in neocortex. , 2009, Annual review of neuroscience.

[16]  C. Gilbert,et al.  Perceptual learning and adult cortical plasticity , 2009, The Journal of physiology.

[17]  Colin J. Akerman,et al.  In Vivo Spike-Timing-Dependent Plasticity in the Optic Tectum of Xenopus Laevis , 2010, Front. Syn. Neurosci..

[18]  R. Huganir,et al.  Phosphorylation of AMPA Receptors Is Required for Sensory Deprivation-Induced Homeostatic Synaptic Plasticity , 2011, PloS one.

[19]  A. Kirkwood,et al.  Pull-Push Neuromodulation of LTP and LTD Enables Bidirectional Experience-Induced Synaptic Scaling in Visual Cortex , 2012, Neuron.

[20]  Alfredo Kirkwood,et al.  Dark Exposure Extends the Integration Window for Spike-Timing-Dependent Plasticity , 2012, The Journal of Neuroscience.

[21]  Alfredo Kirkwood,et al.  Adrenergic Gating of Hebbian Spike-Timing-Dependent Plasticity in Cortical Interneurons , 2013, The Journal of Neuroscience.

[22]  C. Gerloff,et al.  Non-invasive brain stimulation in neurological diseases , 2013, Neuropharmacology.

[23]  G. Koch Do Studies on Cortical Plasticity Provide a Rationale for Using Non-Invasive Brain Stimulation as a Treatment for Parkinson’s Disease Patients? , 2013, Front. Neurol..

[24]  Richard L. Huganir,et al.  AMPARs and Synaptic Plasticity: The Last 25 Years , 2013, Neuron.

[25]  M. Ridding,et al.  Non-invasive induction of plasticity in the human cortex: Uses and limitations , 2014, Cortex.