Neocortical Layer 6, A Review

This review attempts to summarise some of the major areas of neocortical research as it pertains to neocortical layer 6. After a brief summary of the development of this intriguing layer, the major pyramidal cell classes to be found in layer 6 are described and compared. The connections made and received by these different classes of neurones are then discussed and the possible functions of these connections, with particular reference to the shaping of responses in visual cortex and thalamus. Inhibition in layer 6 is discussed where appropriate, but not in great detail. Many types of interneurones are to be found in each cortical layer and layer 6 is no exception, but the functions of each type remain to be elucidated (Gonchar et al., 2007).

[1]  J. B. Levitt,et al.  Inhibitory synapse cover on the somata of excitatory neurons in macaque monkey visual cortex. , 2001, Cerebral cortex.

[2]  J. Lund,et al.  Interlaminar connections and pyramidal neuron organisation in the visual cortex, area 17, of the Macaque monkey , 1975 .

[3]  A. Sillito,et al.  Corticothalamic feedback enhances stimulus response precision in the visual system , 2007, Proceedings of the National Academy of Sciences.

[4]  Quanxin Wang,et al.  Multiple Distinct Subtypes of GABAergic Neurons in Mouse Visual Cortex Identified by Triple Immunostaining , 2007, Frontiers in neuroanatomy.

[5]  M. Ishida,et al.  Area- and lamina-specific organization of a neuronal subpopulation defined by expression of latexin in the rat cerebral cortex , 1999, Neuroscience.

[6]  Björn Granseth,et al.  Paired pulse facilitation of corticogeniculate EPSCs in the dorsal lateral geniculate nucleus of the rat investigated in vitro , 2002, The Journal of physiology.

[7]  Alex M Thomson,et al.  Excitatory connections made by presynaptic cortico-cortical pyramidal cells in layer 6 of the neocortex. , 2005, Cerebral cortex.

[8]  R. Reid,et al.  Receptive field structure varies with layer in the primary visual cortex , 2005, Nature Neuroscience.

[9]  H. Supèr,et al.  The early development of thalamocortical and corticothalamic projections in the mouse , 2000, Anatomy and Embryology.

[10]  S. Sherman,et al.  Evidence for nonreciprocal organization of the mouse auditory thalamocortical‐corticothalamic projection systems , 2008, The Journal of comparative neurology.

[11]  R. Guillery.  Anatomical pathways that link perception and action. , 2005, Progress in brain research.

[12]  T. Wiesel,et al.  Patterns of synaptic input to layer 4 of cat striate cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  R. Reid,et al.  Synaptic Interactions between Thalamic Inputs to Simple Cells in Cat Visual Cortex , 2000, The Journal of Neuroscience.

[14]  P. C. Murphy,et al.  Comparison of the Laminar Distribution of Input from Areas 17 and 18 of the Visual Cortex to the Lateral Geniculate Nucleus of the Cat , 2000, The Journal of Neuroscience.

[15]  J. Deuchars,et al.  Properties of single axon excitatory postsynaptic potentials elicited in spiny interneurons by action potentials in pyramidal neurons in slices of rat neocortex , 1995, Neuroscience.

[16]  Zhen Huang.  Molecular regulation of neuronal migration during neocortical development , 2009, Molecular and Cellular Neuroscience.

[17]  Naoum P. Issa,et al.  The Critical Period for Ocular Dominance Plasticity in the Ferret’s Visual Cortex , 1999, The Journal of Neuroscience.

[18]  A. Thomson,et al.  Release‐independent depression at pyramidal inputs onto specific cell targets: dual recordings in slices of rat cortex , 1999, The Journal of physiology.

[19]  M. Hibi,et al.  Formation and patterning of the forebrain and olfactory system by zinc‐finger genes Fezf1 and Fezf2 , 2009, Development, growth & differentiation.

[20]  M. Sur,et al.  Layer-specific programs of development in neocortical projection neurons. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[21]  D. Godwin,et al.  Differential response dynamics of corticothalamic glutamatergic synapses in the lateral geniculate nucleus and thalamic reticular nucleus , 2006, Neuroscience.

[22]  H. Markram,et al.  Differential signaling via the same axon of neocortical pyramidal neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[23]  P. Rakic.  Evolution of the neocortex: Perspective from developmental biology , 2010 .

[24]  Edward M Callaway,et al.  Local connections to specific types of layer 6 neurons in the rat visual cortex. , 2006, Journal of neurophysiology.

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

[26]  J. B. Levitt,et al.  Connections between the pulvinar complex and cytochrome oxidase-defined compartments in visual area V2 of macaque monkey , 2004, Experimental Brain Research.

[27]  B. Connors,et al.  Short-term dynamics of thalamocortical and intracortical synapses onto layer 6 neurons in neocortex. , 2002, Journal of neurophysiology.

[28]  Alex M Thomson,et al.  Binomial parameters differ across neocortical layers and with different classes of connections in adult rat and cat neocortex , 2007, Proceedings of the National Academy of Sciences.

[29]  M. Deschenes,et al.  Corticothalamic projections from layer 5 of the vibrissal barrel cortex in the rat , 2000, The Journal of comparative neurology.

[30]  P. Rakić,et al.  Mechanisms of cortical development: a view from mutations in mice. , 1978, Annual review of neuroscience.

[31]  M. Deschenes,et al.  Corticothalamic Projections from the Cortical Barrel Field to the Somatosensory Thalamus in Rats: A Single‐fibre Study Using Biocytin as an Anterograde Tracer , 1995, The European journal of neuroscience.

[32]  Charles D. Gilbert,et al.  The Role of Horizontal Connections in Generating Long Receptive Fields in the Cat Visual Cortex , 1989, The European journal of neuroscience.

[33]  A. Thomson,et al.  Functional Maps of Neocortical Local Circuitry , 2007, Front. Neurosci..

[34]  Yun Wang,et al.  Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2-5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro. , 2002, Cerebral cortex.

[35]  Alain Destexhe,et al.  Modelling corticothalamic feedback and the gating of the thalamus by the cerebral cortex , 2000, Journal of Physiology-Paris.

[36]  Qingbo Wang,et al.  Feedforward Excitation and Inhibition Evoke Dual Modes of Firing in the Cat's Visual Thalamus during Naturalistic Viewing , 2007, Neuron.

[37]  D. Fitzpatrick.  The functional organization of local circuits in visual cortex: insights from the study of tree shrew striate cortex. , 1996, Cerebral cortex.

[38]  Martin Deschênes,et al.  The organization of corticothalamic projections: reciprocity versus parity , 1998, Brain Research Reviews.

[39]  J. Lund,et al.  Local circuit neurons of macaque monkey striate cortex: III. Neurons of laminae 4B, 4A, and 3B , 1997, The Journal of comparative neurology.

[40]  H. Jones,et al.  The Length – Response Properties of Cells in the Feline Perigeniculate Nucleus , 1994, The European journal of neuroscience.

[41]  H. Ojima.  Terminal morphology and distribution of corticothalamic fibers originating from layers 5 and 6 of cat primary auditory cortex. , 1994, Cerebral cortex.

[42]  Y. Kubota,et al.  Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  E. Callaway.  Local circuits in primary visual cortex of the macaque monkey. , 1998, Annual review of neuroscience.

[44]  D. Simons,et al.  Circuit dynamics and coding strategies in rodent somatosensory cortex. , 2000, Journal of neurophysiology.

[45]  J. Rossier,et al.  Properties of bipolar VIPergic interneurons and their excitation by pyramidal neurons in the rat neocortex , 1998, The European journal of neuroscience.

[46]  A. Sillito,et al.  A re-appraisal of the role of layer VI of the visual cortex in the generation of cortical end inhibition , 2004, Experimental Brain Research.

[47]  Stephane A. Roy,et al.  Coincidence Detection or Temporal Integration? What the Neurons in Somatosensory Cortex Are Doing , 2001, The Journal of Neuroscience.

[48]  A. Thomson,et al.  Postsynaptic pyramidal target selection by descending layer III pyramidal axons: dual intracellular recordings and biocytin filling in slices of rat neocortex , 1998, Neuroscience.

[49]  S. Hughes,et al.  Synchronized Oscillations at α and θ Frequencies in the Lateral Geniculate Nucleus , 2004, Neuron.

[50]  K E Binns,et al.  Kainate receptor (GluR5)‐mediated disinhibition of responses in rat ventrobasal thalamus allows a novel sensory processing mechanism , 2003, The Journal of physiology.

[51]  S. Sherman,et al.  Thalamic relays and cortical functioning. , 2005, Progress in brain research.

[52]  B. Connors,et al.  VPM and PoM nuclei of the rat somatosensory thalamus: intrinsic neuronal properties and corticothalamic feedback. , 2007, Cerebral cortex.

[53]  Jochen F. Staiger,et al.  Recurrent axon collaterals of corticothalamic projection neurons in rat primary somatosensory cortex contribute to excitatory and inhibitory feedback-loops , 1996, Anatomy and Embryology.

[54]  J. Bourassa,et al.  Corticothalamic projections from the primary visual cortex in rats: a single fiber study using biocytin as an anterograde tracer , 1995, Neuroscience.

[55]  P. C. Murphy,et al.  Feedback connections to the lateral geniculate nucleus and cortical response properties. , 1999, Science.

[56]  S. Murray Sherman,et al.  Modulator Property of the Intrinsic Cortical Projection from Layer 6 to Layer 4 , 2009, Front. Syst. Neurosci..

[57]  R. Kötter,et al.  Cell Type-Specific Circuits of Cortical Layer IV Spiny Neurons , 2003, The Journal of Neuroscience.

[58]  K. Zilles,et al.  Distribution of GABAergic Elements Postsynaptic to Ventroposteromedial Thalamic Projections in Layer IV of Rat Barrel Cortex , 1996, The European journal of neuroscience.

[59]  E. G. Jones,et al.  Viewpoint: the core and matrix of thalamic organization , 1998, Neuroscience.

[60]  A. Sillito,et al.  Functional alignment of feedback effects from visual cortex to thalamus , 2006, Nature Neuroscience.

[61]  C. Shatz,et al.  Subplate neurons pioneer the first axon pathway from the cerebral cortex. , 1989, Science.

[62]  Alex M Thomson,et al.  Layer 6 cortico-thalamic pyramidal cells preferentially innervate interneurons and generate facilitating EPSPs. , 2006, Cerebral cortex.

[63]  U. Eysel,et al.  Inverse correlation of firing patterns of single topographically matched perigeniculate neurons and cat dorsal lateral geniculate relay cells , 1998, Visual Neuroscience.

[64]  J. Deuchars,et al.  Large, deep layer pyramid-pyramid single axon EPSPs in slices of rat motor cortex display paired pulse and frequency-dependent depression, mediated presynaptically and self-facilitation, mediated postsynaptically. , 1993, Journal of neurophysiology.

[65]  T. Powell,et al.  The cortical projection of the ventroposterior nucleus of the thalamus in the cat. , 1969, Brain research.

[66]  S. Hughes,et al.  Synchronized oscillations at alpha and theta frequencies in the lateral geniculate nucleus. , 2004, Neuron.

[67]  Alex M Thomson,et al.  Dynamic properties of excitatory synaptic connections involving layer 4 pyramidal cells in adult rat and cat neocortex. , 2007, Cerebral cortex.

[68]  J. C. Anderson,et al.  Map of the synapses formed with the dendrites of spiny stellate neurons of cat visual cortex , 1994, The Journal of comparative neurology.

[69]  D. Fitzpatrick,et al.  The sublaminar organization of corticogeniculate neurons in layer 6 of macaque striate cortex , 1994, Visual Neuroscience.

[70]  A. Cowey,et al.  Combined golgi and electron microscopic study on the synapses formed by double bouquet cells in the visual cortex of the cat and monkey , 1981, The Journal of comparative neurology.

[71]  Bert Sakmann,et al.  Driver or Coincidence Detector: Modal Switch of a Corticothalamic Giant Synapse Controlled by Spontaneous Activity and Short-Term Depression , 2008, The Journal of Neuroscience.

[72]  George L. Gerstein,et al.  Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex , 1994, Nature.

[73]  E. G. Jones,et al.  Differences in quantal amplitude reflect GluR4- subunit number at corticothalamic synapses on two populations of thalamic neurons , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[74]  J. Brumberg,et al.  Morphological heterogeneity of layer VI neurons in mouse barrel cortex , 2009, The Journal of comparative neurology.

[75]  A. Parker,et al.  Local circuit neurons of macaque monkey striate cortex: II. Neurons of laminae 5B and 6 , 1988, The Journal of comparative neurology.

[76]  A. Thomson.  Activity‐dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro , 1997, The Journal of physiology.

[77]  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.

[78]  B. Sakmann,et al.  Cortex Is Driven by Weak but Synchronously Active Thalamocortical Synapses , 2006, Science.

[79]  E. Callaway,et al.  Ocular dominance columns and local projections of layer 6 pyramidal neurons in macaque primary visual cortex , 1997, Visual Neuroscience.

[80]  P. Rakić,et al.  Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain , 1990, The Journal of comparative neurology.

[81]  E Kaplan,et al.  Contrast affects the transmission of visual information through the mammalian lateral geniculate nucleus. , 1987, The Journal of physiology.

[82]  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.

[83]  J. Olson,et al.  Regulation of Thalamocortical Patterning and Synaptic Maturation by NeuroD2 , 2006, Neuron.

[84]  J. Bolz,et al.  Functional specificity of a long-range horizontal connection in cat visual cortex: a cross-correlation study , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[85]  W. Bai,et al.  Chemically defined feedback connections from infragranular layers of sensory association cortices in the rat , 2004, Neuroscience.

[86]  P. C. Murphy,et al.  Functional morphology of the feedback pathway from area 17 of the cat visual cortex to the lateral geniculate nucleus , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[87]  M. Ishida,et al.  Corticocortical associative neurons expressing latexin: specific cortical connectivity formed in vivo and in vitro. , 1999, Cerebral cortex.

[88]  L. Martinez,et al.  Completing the Corticofugal Loop: A Visual Role for the Corticogeniculate Type 1 Metabotropic Glutamate Receptor , 2002, The Journal of Neuroscience.

[89]  A. Sillito,et al.  The length summation properties of layer VI cells in the visual cortex and hypercomplex cell end zone inhibition , 2004, Experimental Brain Research.

[90]  C. A. Gallagher,et al.  Ascending Projections of Simple and Complex Cells in Layer 6 of the Cat Striate Cortex , 1998, The Journal of Neuroscience.

[91]  R. Guillery,et al.  Patterns of synaptic contact upon individually labeled large cells of the dorsal lateral geniculate nucleus of the cat , 1984, Neuroscience.

[92]  M. Deschenes,et al.  Intracortical Axonal Projections of Lamina VI Cells of the Primary Somatosensory Cortex in the Rat: A Single-Cell Labeling Study , 1997, The Journal of Neuroscience.

[93]  Martin Deschênes,et al.  A New Thalamic Pathway of Vibrissal Information Modulated by the Motor Cortex , 2007, The Journal of Neuroscience.

[94]  M. Ishida,et al.  Distinct neuronal populations specified to form corticocortical and corticothalamic projections from layer VI of developing cerebral cortex , 2002, Neuroscience.

[95]  M. Castro-Alamancos,et al.  Properties of primary sensory (lemniscal) synapses in the ventrobasal thalamus and the relay of high-frequency sensory inputs. , 2002, Journal of neurophysiology.

[96]  M. Miyata,et al.  Different composition of glutamate receptors in corticothalamic and lemniscal synaptic responses and their roles in the firing responses of ventrobasal thalamic neurons in juvenile mice , 2006, The Journal of physiology.

[97]  T. Powell,et al.  The projection of the auditory cortex upon the diencephalon and brain stem in the cat. , 1969, Brain research.

[98]  V. Crunelli,et al.  The impact of corticothalamic feedback on the output dynamics of a thalamocortical neurone model: the role of synapse location and metabotropic glutamate receptors , 2003, Neuroscience.

[99]  J. Lund,et al.  Anatomical organization of macaque monkey striate visual cortex. , 1988, Annual review of neuroscience.

[100]  J. B. Levitt,et al.  Independence and merger of thalamocortical channels within macaque monkey primary visual cortex: Anatomy of interlaminar projections , 1994, Visual Neuroscience.

[101]  D. Fitzpatrick,et al.  Specificity in the axonal connections of layer VI neurons in tree shrew striate cortex: evidence for distinct granular and supragranular systems , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[102]  A. Sillito,et al.  Spatial frequency tuning of orientation‐discontinuity‐sensitive corticofugal feedback to the cat lateral geniculate nucleus. , 1996, The Journal of physiology.

[103]  J. Rubenstein,et al.  Tbr1 Regulates Differentiation of the Preplate and Layer 6 , 2001, Neuron.

[104]  T. Salt,et al.  Characterization of sensory and corticothalamic excitatory inputs to rat thalamocortical neurones in vitro , 1998, The Journal of physiology.

[105]  F. Polleux,et al.  Close Homolog of L1 and Neuropilin 1 Mediate Guidance of Thalamocortical Axons at the Ventral Telencephalon , 2007, The Journal of Neuroscience.

[106]  R. Guillery,et al.  Functional organization of thalamocortical relays. , 1996, Journal of neurophysiology.

[107]  G. Orban,et al.  Learning to See the Difference Specifically Alters the Most Informative V4 Neurons , 2006, The Journal of Neuroscience.

[108]  E Friauf,et al.  Functional synaptic circuits in the subplate during fetal and early postnatal development of cat visual cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[109]  V. Lefebvre,et al.  SOX5 postmitotically regulates migration, postmigratory differentiation, and projections of subplate and deep-layer neocortical neurons , 2008, Proceedings of the National Academy of Sciences.

[110]  H. Jones,et al.  The length‐response properties of cells in the feline dorsal lateral geniculate nucleus. , 1991, The Journal of physiology.

[111]  A. M. Sillito,et al.  Orientation sensitive elements in the corticofugal influence on centre-surround interactions in the dorsal lateral geniculate nucleus , 1993, Experimental Brain Research.

[112]  M. Deschenes,et al.  Projections to layer VI of the posteromedial barrel field in the rat: a reappraisal of the role of corticothalamic pathways. , 1998, Cerebral cortex.

[113]  J. Deuchars,et al.  Innervation of burst firing spiny interneurons by pyramidal cells in deep layers of rat somatomotor cortex: Paired intracellular recordings with biocytin filling , 1995, Neuroscience.

[114]  E. Callaway,et al.  Development of axonal arbors of layer 6 pyramidal neurons in ferret primary visual cortex , 1996, The Journal of comparative neurology.

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

[116]  C. Gilbert,et al.  Generation of end-inhibition in the visual cortex via interlaminar connections , 1986, Nature.