Local connections to specific types of layer 6 neurons in the rat visual cortex.

Because layer 6 of the cerebral cortex receives direct thalamic input and provides projections back to the thalamus, it is in a unique position to influence thalamocortical interactions. Different types of layer 6 pyramidal neurons provide output to different thalamic nuclei, and it is therefore of interest to understand the sources of functional input to these neurons. We studied the morphologies and local excitatory input to individual layer 6 neurons in rat visual cortex by combining intracellular labeling and recording with laser-scanning photostimulation. As in previous photostimulation studies, we found significant differences in the sources of local excitatory input to different cell types. Most notably, there were differences in local input to neurons that, based on analogy to barrel cortex, are likely to project only to the lateral geniculate nucleus of the thalamus versus those that are likely to also project to the lateral posterior nucleus. The more striking finding, however, was the paucity of superficial layer input to layer 6 neurons in the rat visual cortex, contrasting sharply with layer 6 neurons in the primate visual cortex. These observations provide insight into differences in function between cortical projections to first-order versus higher-order thalamic nuclei and also show that these circuits can be organized differently in different species.

[1]  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.

[2]  Lawrence C. Katz,et al.  Scanning laser photostimulation: a new approach for analyzing brain circuits , 1994, Journal of Neuroscience Methods.

[3]  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.

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

[5]  B. Finlay,et al.  Linked regularities in the development and evolution of mammalian brains. , 1995, Science.

[6]  E M Callaway,et al.  Layer-Specific Input to Distinct Cell Types in Layer 6 of Monkey Primary Visual Cortex , 2001, The Journal of Neuroscience.

[7]  Edward M Callaway,et al.  Diversity and Cell Type Specificity of Local Excitatory Connections to Neurons in Layer 3B of Monkey Primary Visual Cortex , 2000, Neuron.

[8]  E. Callaway,et al.  Photostimulation using caged glutamate reveals functional circuitry in living brain slices. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[9]  J. Olavarria,et al.  Widespread callosal connections in infragranular visual cortex of the rat , 1983, Brain Research.

[10]  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.

[11]  R. Guillery,et al.  Thalamic Relay Functions and Their Role in Corticocortical Communication Generalizations from the Visual System , 2002, Neuron.

[12]  M. Herkenham.  Laminar organization of thalamic projections to the rat neocortex. , 1980, Science.

[13]  E. Callaway,et al.  Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons , 2000, Nature Neuroscience.

[14]  L. Benevento,et al.  A comparison of the organization of the projections of the dorsal lateral geniculate nucleus, the inferior pulvinar and adjacent lateral pulvinar to primary visual cortex (area 17) in the macaque monkey , 1979, Brain Research.

[15]  E. Callaway,et al.  Functional Streams and Local Connections of Layer 4C Neurons in Primary Visual Cortex of the Macaque Monkey , 1998, The Journal of Neuroscience.

[16]  J. Lund,et al.  The termination of callosal fibers in the paravisual cortex of the rat. , 1970, Brain research.

[17]  E. Callaway,et al.  Excitatory cortical neurons form fine-scale functional networks , 2005, Nature.

[18]  Partha P. Mitra,et al.  Scalable architecture in mammalian brains , 2001, Nature.

[19]  Farran Briggs,et al.  Laminar patterns of local excitatory input to layer 5 neurons in macaque primary visual cortex. , 2005, Cerebral cortex.

[20]  C. Gilbert.  Microcircuitry of the visual cortex. , 1983, Annual review of neuroscience.

[21]  A. Hendrickson,et al.  The distribution of pulvinar terminals in visual areas 17 and 18 of the monkey , 1977, Brain Research.

[22]  E. Callaway,et al.  Convergence of magno- and parvocellular pathways in layer 4B of macaque primary visual cortex , 1996, Nature.

[23]  E. Callaway,et al.  Cytochrome-oxidase blobs and intrinsic horizontal connections of layer 2/3 pyramidal neurons in primate V1 , 1998, Visual Neuroscience.

[24]  T. Wiesel,et al.  Functional organization of the visual cortex. , 1983, Progress in brain research.

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

[26]  G. Snyder,et al.  A comparison of the electrophysiological properties of morphologically identified cells in layers 5B and 6 of the rat neocortex , 1992, Neuroscience.

[27]  R. Kötter,et al.  Layer-Specific Intracolumnar and Transcolumnar Functional Connectivity of Layer V Pyramidal Cells in Rat Barrel Cortex , 2001, The Journal of Neuroscience.

[28]  J. Lund,et al.  The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase , 1975, The Journal of comparative neurology.

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