Modulator Property of the Intrinsic Cortical Projection from Layer 6 to Layer 4

Layer 4 of the sensory neocortex receives widespread convergent inputs from thalamic, intracortical, and corticocortical sources. Yet, the relative information bearing roles for most of these pathways remain largely undefined. Here we show that the intracortical projections from layer 6 to layer 4 exhibit a physiological property that is consistent with a modulator role. Using in vitro slice preparations of the auditory and somatosensory cortices, we found that electrical stimulation or photostimulation of layer 6 elicits a prolonged depolarizing response that is attributable to the activation of group 1 metabotropic glutamate receptors. These results complement the known physiological properties of the layer 6 to layer 4 pathway, and further suggest that this pathway is not a principle conduit for information flow, but rather acts as a modulator of cortical activity.

[1]  J. Winer,et al.  Auditory thalamocortical projections in the cat: Laminar and areal patterns of input , 2000, The Journal of comparative neurology.

[2]  S. Sherman,et al.  Glutamatergic inhibition in sensory neocortex. , 2009, Cerebral cortex.

[3]  R. Metherate,et al.  Auditory thalamocortical transmission is reliable and temporally precise. , 2005, Journal of neurophysiology.

[4]  S. Sherman,et al.  Metabotropic glutamate receptors switch visual response mode of lateral geniculate nucleus cells from burst to tonic. , 1996, Journal of neurophysiology.

[5]  R. Douglas,et al.  A Quantitative Map of the Circuit of Cat Primary Visual Cortex , 2004, The Journal of Neuroscience.

[6]  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.

[7]  R. Reid,et al.  Specificity of monosynaptic connections from thalamus to visual cortex , 1995, Nature.

[8]  K. Martin,et al.  Intracortical excitation of spiny neurons in layer 4 of cat striate cortex in vitro. , 1999, Cerebral cortex.

[9]  K. Reymann,et al.  Comparing the role of metabotropic glutamate receptors in long-term potentiation and in learning and memory , 1996, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[10]  L. Martinez,et al.  Circuits that build visual cortical receptive fields , 2006, Trends in Neurosciences.

[11]  R. Luján Exploring the Thalamus and its Role in Cortical Function, S.M. Sherman, R.W. Guillery (Eds.). The MIT Press (2006), ISBN: 0-262-19532-1 , 2007 .

[12]  K. Martin,et al.  Excitatory synaptic inputs to spiny stellate cells in cat visual cortex , 1996, Nature.

[13]  P. H. Smith,et al.  Effects of paired-pulse and repetitive stimulation on neurons in the rat medial geniculate body , 2002, Neuroscience.

[14]  D. Ferster,et al.  Orientation selectivity of thalamic input to simple cells of cat visual cortex , 1996, Nature.

[15]  B. Connors,et al.  Efficacy of Thalamocortical and Intracortical Synaptic Connections Quanta, Innervation, and Reliability , 1999, Neuron.

[16]  Karel Svoboda,et al.  Circuit Analysis of Experience-Dependent Plasticity in the Developing Rat Barrel Cortex , 2003, Neuron.

[17]  Immunohistochemical Localization of Metabotropic and Ionotropic Glutamate Receptors in the Mouse Brain , 1993, Annals of the New York Academy of Sciences.

[18]  S. Sherman,et al.  Ultrastructural Localization Suggests that Retinal and Cortical Inputs Access Different Metabotropic Glutamate Receptors in the Lateral Geniculate Nucleus , 1996, The Journal of Neuroscience.

[19]  D. Schoepp,et al.  Regulation of Neurotransmitter Release by Metabotropic Glutamate Receptors , 2000, Journal of neurochemistry.

[20]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[21]  J. C. Anderson,et al.  Polyneuronal innervation of spiny stellate neurons in cat visual cortex , 1994, The Journal of comparative neurology.

[22]  D. McCormick,et al.  Corticothalamic activation modulates thalamic firing through glutamate "metabotropic" receptors. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[23]  A. Burette,et al.  Immunolocalization of mGluR1α in specific populations of local circuit neurons in the cerebral cortex , 2000, Brain Research.

[24]  M. Bickford,et al.  Two distinct types of corticothalamic EPSPs and their contribution to short-term synaptic plasticity. , 2003, Journal of neurophysiology.

[25]  C. Hölscher Metabotropic glutamate receptors control gating of spike transmission in the hippocampus area CA1 , 2002, Pharmacology Biochemistry and Behavior.

[26]  Brendon O. Watson,et al.  A visual thalamocortical slice , 2006, Nature Methods.

[27]  A. Fairén,et al.  Differential distribution of group I metabotropic glutamate receptors during rat cortical development. , 2002, Cerebral cortex.

[28]  S. Sherman,et al.  Synaptic properties of thalamic and intracortical inputs to layer 4 of the first- and higher-order cortical areas in the auditory and somatosensory systems. , 2008, Journal of neurophysiology.

[29]  K. Martin,et al.  Termination of the geniculocortical projection in the striate cortex of macaque monkey: A quantitative immunoelectron microscopic study , 2000, The Journal of comparative neurology.

[30]  S Murray Sherman,et al.  Different topography of the reticulothalmic inputs to first- and higher-order somatosensory thalamic relays revealed using photostimulation. , 2007, Journal of neurophysiology.

[31]  R. Guillery,et al.  On the actions that one nerve cell can have on another: distinguishing "drivers" from "modulators". , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[32]  S. Grossberg,et al.  Towards a theory of the laminar architecture of cerebral cortex: computational clues from the visual system. , 2003, Cerebral cortex.

[33]  Christoph E Schreiner,et al.  Concurrent tonotopic processing streams in auditory cortex. , 2004, Cerebral cortex.

[34]  I. Reichova,et al.  Somatosensory corticothalamic projections: distinguishing drivers from modulators. , 2004, Journal of neurophysiology.