Morphological Substrates for Parallel Streams of Corticogeniculate Feedback Originating in Both V1 and V2 of the Macaque Monkey

Corticothalamic circuits are essential for reciprocal information exchange between the thalamus and cerebral cortex. Nevertheless, the role of corticothalamic circuits in sensory processing remains a mystery. In the visual system, afferents from retina to the lateral geniculate nucleus (LGN) and from LGN to primary visual cortex (V1) are organized into functionally distinct parallel processing streams. Physiological evidence suggests corticogeniculate feedback may be organized into parallel streams; however, little is known about the diversity of corticogeniculate neurons, their local computations, or the structure-function relationship among corticogeniculate neurons. We used a virus-mediated approach to label and reconstruct the complete dendritic and local axonal arbors of identified corticogeniculate neurons in the macaque monkey. Our results reveal morphological substrates for parallel streams of corticogeniculate feedback based on distinct classes of neurons in V1 and V2. These results support the hypothesis that distinct populations of feedback neurons provide independent and unique information to the LGN.

[1]  R. Guillery,et al.  Exploring the Thalamus and Its Role in Cortical Function , 2005 .

[2]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[3]  Farran Briggs,et al.  Corticogeniculate feedback and visual processing in the primate , 2011, The Journal of physiology.

[4]  T. Tsumoto,et al.  Three groups of cortico‐geniculate neurons and their distribution in binocular and monocular segments of cat striate cortex , 1980, The Journal of comparative neurology.

[5]  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.

[6]  S. Sherman,et al.  Relative numbers of cortical and brainstem inputs to the lateral geniculate nucleus. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[7]  R. W. Güillery.  A quantitative study of synaptic interconnections in the dorsal lateral geniculate nucleus of the cat , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[8]  E. Jones,et al.  Thalamic organization and function after Cajal. , 2002, Progress in brain research.

[9]  Michael W. Miller.  Maturation of rat visual cortex: IV. The generation, migration, morphogenesis, and connectivity of atypically oriented pyramidal neurons , 1988, The Journal of comparative neurology.

[10]  D. Raczkowski,et al.  Sublaminar organization within layer VI of the striate cortex in Galago , 1990, The Journal of comparative neurology.

[11]  C. Gilbert,et al.  The projections of cells in different layers of the cat's visual cortex , 1975, The Journal of comparative neurology.

[12]  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.

[13]  R. L. Thorndike.  Who belongs in the family? , 1953 .

[14]  A W Roe,et al.  Specificity of color connectivity between primate V1 and V2. , 1999, Journal of neurophysiology.

[15]  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.

[16]  K. Rockland.  Further evidence for two types of corticopulvinar neurons. , 1994, Neuroreport.

[17]  W. le Gros Clark.  The cells of Meynert in the visual cortex of the monkey. , 1942, Journal of anatomy.

[18]  D. Hubel,et al.  Anatomy and physiology of a color system in the primate visual cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  W. Usrey,et al.  Emerging views of corticothalamic function , 2008, Current Opinion in Neurobiology.

[20]  Ian R. Wickersham,et al.  Retrograde neuronal tracing with a deletion-mutant rabies virus , 2007, Nature Methods.

[21]  Farran Briggs,et al.  A Fast, Reciprocal Pathway between the Lateral Geniculate Nucleus and Visual Cortex in the Macaque Monkey , 2007, The Journal of Neuroscience.

[22]  E. Jones.  Calcium channels in higher-level brain function , 2007, Proceedings of the National Academy of Sciences.

[23]  R W Guillery,et al.  Structure and connections of the thalamic reticular nucleus: Advancing views over half a century , 2003, The Journal of comparative neurology.

[24]  Shaul Hestrin,et al.  Layer 6 Corticothalamic Neurons Activate a Cortical Output Layer, Layer 5a , 2014, The Journal of Neuroscience.

[25]  James H. Marshel,et al.  New rabies virus variants for monitoring and manipulating activity and gene expression in defined neural circuits. , 2011, Neuron.

[26]  S. Sherman,et al.  Immunocytochemistry and distribution of parabrachial terminals in the lateral geniculate nucleus of the cat: A comparison with corticogeniculate terminals , 1997, The Journal of comparative neurology.

[27]  Farran Briggs,et al.  Temporal properties of feedforward and feedback pathways between the thalamus and visual cortex in the ferret. , 2005, Thalamus & related systems.

[28]  L C Katz,et al.  Local circuitry of identified projection neurons in cat visual cortex brain slices , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  E. Callaway.  Transneuronal circuit tracing with neurotropic viruses , 2008, Current Opinion in Neurobiology.

[30]  V. Casagrande,et al.  Distinct patterns of corticogeniculate feedback to different layers of the lateral geniculate nucleus , 2014, Eye and brain.

[31]  M. Conley,et al.  Functional organization of the ventral lateral geniculate complex of the tree shrew (Tupaia belangeri): II. Connections with the cortex, thalamus, and brainstem , 1993, The Journal of comparative neurology.

[32]  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.

[33]  W. Usrey,et al.  Parallel Processing in the Corticogeniculate Pathway of the Macaque Monkey , 2009, Neuron.

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

[35]  A. Sillito,et al.  Differential properties of cells in the feline primary visual cortex providing the corticofugal feedback to the lateral geniculate nucleus and visual claustrum , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  A. Harvey.  Characteristics of corticothalamic neurons in area 17 of the cat , 1978, Neuroscience Letters.

[37]  T. Powell,et al.  The basal dendrites of Meynert cells in the striate cortex of the monkey , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[38]  Vivien A Casagrande,et al.  Organization of the feedback pathway from striate cortex (V1) to the lateral geniculate nucleus (LGN) in the owl monkey (Aotus trivirgatus) , 2002, The Journal of comparative neurology.

[39]  Warren M. Grill.  Exploring the Thalamus and Its Role in Cortical Function.Second Edition.ByS Murray Shermanand, R W Guillery.Cambridge (Massachusetts): MIT Press.$65.00. xxiii + 484 p; ill.; index. ISBN: 0‐262‐19532‐1. 2006. , 2007 .

[40]  J. Kaas,et al.  Projections from cortical visual areas 17, 18, and MT onto the dorsal lateral geniculate nucleus in owl monkeys , 1977, The Journal of comparative neurology.

[41]  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.

[42]  H. Swadlow,et al.  Corticogeniculate neurons, corticotectal neurons, and suspected interneurons in visual cortex of awake rabbits: receptive-field properties, axonal properties, and effects of EEG arousal. , 1987, Journal of neurophysiology.

[43]  Lawrence C. Sincich,et al.  The circuitry of V1 and V2: integration of color, form, and motion. , 2005, Annual review of neuroscience.

[44]  le Gros Clark We,et al.  The cells of Meynert in the visual cortex of the monkey. , 1942 .

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

[46]  E. Callaway,et al.  Contributions of individual layer 6 pyramidal neurons to local circuitry in macaque primary visual cortex , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  James H. Marshel,et al.  New Rabies Virus Variants for Monitoring and Manipulating Activity and Gene Expression in Defined Neural Circuits , 2011, Neuron.

[48]  J. Rossier,et al.  Classification of fusiform neocortical interneurons based on unsupervised clustering. , 2000, Proceedings of the National Academy of Sciences of the United States of America.