Associations of Unilateral Whisker and Olfactory Signals Induce Synapse Formation and Memory Cell Recruitment in Bilateral Barrel Cortices: Cellular Mechanism for Unilateral Training Toward Bilateral Memory

Somatosensory signals and operative skills learned by unilateral limbs can be retrieved bilaterally. In terms of cellular mechanism underlying this unilateral learning toward bilateral memory, we hypothesized that associative memory cells in bilateral cortices and synapse innervations between them were produced. In the examination of this hypothesis, we have observed that paired unilateral whisker and odor stimulations led to odorant-induced whisker motions in bilateral sides, which were attenuated by inhibiting the activity of barrel cortices. In the mice that showed bilateral cross-modal responses, the neurons in both sides of barrel cortices became to encode this new odor signal alongside the innate whisker signal. Axon projections and synapse formations from the barrel cortex, which was co-activated with the piriform cortex, toward its contralateral barrel cortex (CBC) were upregulated. Glutamatergic synaptic transmission in bilateral barrel cortices was upregulated and GABAergic synaptic transmission was downregulated. The associative activations of the sensory cortices facilitate new axon projection, glutamatergic synapse formation and GABAergic synapse downregulation, which drive the neurons to be recruited as associative memory cells in the bilateral cortices. Our data reveal the productions of associative memory cells and synapse innervations in bilateral sensory cortices for unilateral training toward bilateral memory.

[1]  Alison L. Barth,et al.  Ipsilateral Whiskers Suppress Experience-Dependent Plasticity in the Barrel Cortex , 2007, The Journal of Neuroscience.

[2]  S. F. Witelson The brain connection: the corpus callosum is larger in left-handers. , 1985, Science.

[3]  M. Diamond,et al.  Whisker sensory system – From receptor to decision , 2013, Progress in Neurobiology.

[4]  Jin-Hui Wang,et al.  Gain and fidelity of transmission patterns at cortical excitatory unitary synapses improve spike encoding , 2008, Journal of Cell Science.

[5]  W. Regehr,et al.  Short-term synaptic plasticity. , 2002, Annual review of physiology.

[6]  Mathew E. Diamond,et al.  The Cortical Distribution of Sensory Memories , 2001, Neuron.

[7]  G. Geffen,et al.  Corpus callosum surgery and recent memory. A review. , 1989, Brain : a journal of neurology.

[8]  W. Brown,et al.  Verbal learning and memory in agenesis of the corpus callosum , 2014, Neuropsychologia.

[9]  N. Weinberger Specific long-term memory traces in primary auditory cortex , 2004, Nature Reviews Neuroscience.

[10]  Yan Zhu,et al.  Upregulation of excitatory neurons and downregulation of inhibitory neurons in barrel cortex are associated with loss of whisker inputs , 2013, Molecular Brain.

[11]  B. Ye,et al.  The Functional Upregulation of Piriform Cortex Is Associated with Cross-Modal Plasticity in Loss of Whisker Tactile Inputs , 2012, PloS one.

[12]  C. W. Wong Corpus callosum and cerebral laterality in a modular brain model. , 2000, Medical hypotheses.

[13]  Justin A. Harris,et al.  Investigations into the organization of information in sensory cortex , 2003, Journal of Physiology-Paris.

[14]  K. Alloway,et al.  Septal columns in rodent barrel cortex: Functional circuits for modulating whisking behavior , 2004, The Journal of comparative neurology.

[15]  Jin-Hui Wang,et al.  A Portion of Inhibitory Neurons in Human Temporal Lobe Epilepsy are Functionally Upregulated: An Endogenous Mechanism for Seizure Termination , 2015, CNS neuroscience & therapeutics.

[16]  George Paxinos,et al.  The Mouse Brain in Stereotaxic Coordinates , 2001 .

[17]  Wei Lu,et al.  Neurons in the barrel cortex turn into processing whisker and odor signals: a cellular mechanism for the storage and retrieval of associative signals , 2015, Front. Cell. Neurosci..

[18]  Na Chen,et al.  Upregulation of Glutamatergic Receptor-Channels is Associated with Cross-Modal Reflexes Encoded in Barrel Cortex and Piriform Cortex , 2014 .

[19]  Jin-Hui Wang,et al.  Homeostasis established by coordination of subcellular compartment plasticity improves spike encoding , 2008, Journal of Cell Science.

[20]  Jin-Hui Wang,et al.  Input-dependent subcellular localization of spike initiation between soma and axon at cortical pyramidal neurons , 2014, Molecular Brain.

[21]  Concha Bielza,et al.  New insights into the classification and nomenclature of cortical GABAergic interneurons , 2013, Nature Reviews Neuroscience.

[22]  Jens Frahm,et al.  Topography of the human corpus callosum revisited—Comprehensive fiber tractography using diffusion tensor magnetic resonance imaging , 2006, NeuroImage.

[23]  Y Miyashita,et al.  Memory retrieval under the control of the prefrontal cortex. , 1999, Annals of medicine.

[24]  Xiang Zhou,et al.  New Modules Are Added to Vibrissal Premotor Circuitry with the Emergence of Exploratory Whisking , 2013, Neuron.

[25]  R. Pashaie,et al.  Spectral analysis of whisking output via optogenetic modulation of vibrissa cortex in rat , 2012, Biomedical optics express.

[26]  Jin-Hui Wang,et al.  Voltage-independent sodium channels emerge for an expression of activity-induced spontaneous spikes in GABAergic neurons , 2014, Molecular Brain.

[27]  R. Zatorre,et al.  Early Musical Training and White-Matter Plasticity in the Corpus Callosum: Evidence for a Sensitive Period , 2013, The Journal of Neuroscience.

[28]  Y. Kawaguchi Receptor subtypes involved in callosally-induced postsynaptic potentials in rat frontal agranular cortex in vitro , 2005, Experimental Brain Research.

[29]  Dangui Wang,et al.  Barrel cortical neurons and astrocytes coordinately respond to an increased whisker stimulus frequency , 2012, Molecular Brain.

[30]  Yan Zhu,et al.  Sodium channel-mediated intrinsic mechanisms underlying the differences of spike programming among GABAergic neurons. , 2006, Biochemical and biophysical research communications.

[31]  Mark Mayford,et al.  Localization of a Stable Neural Correlate of Associative Memory , 2007, Science.

[32]  Jin-Hui Wang Short-term cerebral ischemia causes the dysfunction of interneurons and more excitation of pyramidal neurons in rats , 2003, Brain Research Bulletin.

[33]  W. Suzuki Associative learning signals in the brain. , 2008, Progress in brain research.

[34]  Khader M Hasan,et al.  Working memory and corpus callosum microstructural integrity after pediatric traumatic brain injury: a diffusion tensor tractography study. , 2013, Journal of neurotrauma.

[35]  Charles F. Stevens Presynaptic function , 2004, Current Opinion in Neurobiology.

[36]  J. Bloedel,et al.  The cerebellum and eye-blink conditioning: learning versus network performance hypotheses , 2009, Neuroscience.

[37]  Jin-Hui Wang,et al.  Physiological synaptic signals initiate sequential spikes at soma of cortical pyramidal neurons , 2011, Molecular Brain.

[38]  Yan Zhu,et al.  Upregulation of Barrel GABAergic Neurons Is Associated with Cross-Modal Plasticity in Olfactory Deficit , 2010, PloS one.

[39]  I. Hasegawa Neural Mechanisms of Memory Retrieval: Role of the Prefrontal Cortex , 2000, Reviews in the neurosciences.

[40]  Geoffrey G Murphy,et al.  Deletion of the Mouse Homolog of KCNAB2, a Gene Linked to Monosomy 1p36, Results in Associative Memory Impairments and Amygdala Hyperexcitability , 2011, The Journal of Neuroscience.

[41]  A. Lansner Associative memory models: from the cell-assembly theory to biophysically detailed cortex simulations , 2009, Trends in Neurosciences.

[42]  Min Sun,et al.  Impaired GABA synthesis, uptake and release are associated with depression-like behaviors induced by chronic mild stress , 2016, Translational psychiatry.

[43]  G. Keppel,et al.  Verbal learning and memory. , 1968, Annual review of psychology.

[44]  Brian Avants,et al.  Characterization of sexual dimorphism in the human corpus callosum , 2003, NeuroImage.

[45]  S. P. Swinnen,et al.  Interactions between brain structure and behavior: The corpus callosum and bimanual coordination , 2014, Neuroscience & Biobehavioral Reviews.

[46]  Stephen Maren,et al.  Pavlovian fear conditioning as a behavioral assay for hippocampus and amygdala function: cautions and caveats , 2008, The European journal of neuroscience.

[47]  J. Disterhoft,et al.  Where is the trace in trace conditioning? , 2008, Trends in Neurosciences.

[48]  Jin-Hui Wang,et al.  Calcium‐calmodulin signalling pathway up‐regulates glutamatergic synaptic function in non‐pyramidal, fast spiking rat hippocampal CA1 neurons , 2001, The Journal of physiology.

[49]  Celine Mateo,et al.  Motor Control by Sensory Cortex , 2010, Science.

[50]  M A Nicolelis,et al.  Bilateral Integration of Whisker Information in the Primary Somatosensory Cortex of Rats , 2001, The Journal of Neuroscience.

[51]  Andrei I Holodny,et al.  Investigating Agenesis of the Corpus Callosum Using Functional MRI: A Study Examining Interhemispheric Coordination of Motor Control , 2011, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[52]  M. Caleo,et al.  The Corpus Callosum and the Visual Cortex: Plasticity Is a Game for Two , 2012, Neural plasticity.

[53]  M. Piercy Studies of the neurological basis of intellectual function. , 1967, Modern trends in neurology.

[54]  Atsushi Miyawaki,et al.  Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain , 2011, Nature Neuroscience.

[55]  C. Petersen,et al.  Long‐range connectivity of mouse primary somatosensory barrel cortex , 2010, The European journal of neuroscience.

[56]  Johannes J. Letzkus,et al.  A disinhibitory microcircuit for associative fear learning in the auditory cortex , 2011, Nature.

[57]  Wei Lu,et al.  Both Glutamatergic and Gabaergic Neurons are Recruited to be Associative Memory Cells , 2016 .

[58]  Michael Davis,et al.  Fear-potentiated startle: A neural and pharmacological analysis , 1993, Behavioural Brain Research.

[59]  H. Killackey,et al.  Evidence for the complementary organization of callosal and thalamic connections within rat somatosensory cortex , 1984, Brain Research.

[60]  Wei Xu,et al.  A Neural Circuit for Memory Specificity and Generalization , 2013, Science.

[61]  E. Ross,et al.  Topography of the Human Corpus Callosum , 1985, Journal of neuropathology and experimental neurology.

[62]  R. R. Miller,et al.  What's elementary about associative learning? , 1997, Annual review of psychology.

[63]  Nathan G. Clack,et al.  Vibrissa-Based Object Localization in Head-Fixed Mice , 2010, The Journal of Neuroscience.

[64]  Kevin D Alloway,et al.  Bilateral projections from rat MI whisker cortex to the neostriatum, thalamus, and claustrum: Forebrain circuits for modulating whisking behavior , 2009, The Journal of comparative neurology.

[65]  M. Lassonde,et al.  Functional consequences of a section of the anterior part of the body of the corpus callosum: evidence from an interhemispheric transcallosal approach , 2012, Journal of Neurology.

[66]  N. Weinberger Associative representational plasticity in the auditory cortex: a synthesis of two disciplines. , 2007, Learning & memory.

[67]  Jin-Hui Wang,et al.  Incoordination among Subcellular Compartments Is Associated with Depression-Like Behavior Induced by Chronic Mild Stress , 2015, The international journal of neuropsychopharmacology.

[68]  B. Schreurs,et al.  Conditioning-specific reflex modification of the rabbit's nictitating membrane response and heart rate: behavioral rules, neural substrates, and potential applications to posttraumatic stress disorder. , 2008, Behavioral neuroscience.

[69]  Y. Miyashita,et al.  Callosal window between prefrontal cortices: cognitive interaction to retrieve long-term memory. , 1998, Science.

[70]  S. Swinnen,et al.  Bimanual coordination and corpus callosum microstructure in young adults with traumatic brain injury: a diffusion tensor imaging study. , 2010, Journal of neurotrauma.

[71]  M. Armstrong‐James,et al.  Bilateral receptive fields of cells in rat Sm1 cortex , 1988, Experimental Brain Research.

[72]  Fengyu Zhang,et al.  mGluR1,5 activation improves network asynchrony and GABAergic synapse attenuation in the amygdala: implication for anxiety-like behavior in DBA/2 mice , 2012, Molecular Brain.