Feedback connections from area MT of the squirrel monkey to areas V1 and V2

Area MT/V5 is reciprocally connected with both V1 and V2; but, despite extensive anatomical and physiological investigations, detailed information on the feedback component of these connections is still not available. The present report uses serial section reconstruction of single axons, labeled by anterograde tracers injected in area MT of squirrel monkeys, to characterize these connections further. As with other feedback systems, MT axons terminating in both areas V1 (n = 9) and V2 (n = 6) are widely divergent. In area V1, MT fields are larger than those from V2 and are about comparable to those from V4 or TEO. Terminations in V1, unlike other feedback connections described so far, terminate in several laminar combinations: only layer 1 (n = 2); only layer 4B (n = 3); layers 1 and 4B (n = 1); and layers 1, 4B, and 6 (n = 3). In V2, they occur mainly in layers 1 and 5 or 6. Terminations have two patterns even within a single axon: strung along collateral segments and grouped within small clusters. There are no apparent differences in the size, shape, or density of terminal specializations in V1 or V2, and, consistently with previous double‐labeling experiments (Kennedy and Bullier [1985] J Neurosci 5:2815–2830), some axons can branch to both areas. This result, along with the laminar evidence for subtypes of feedback connections, argues against an exclusively hierarchical organization based on “pairwise” connectivity. For V1 and MT, there may be directly reciprocal loops between feedforward and feedback projecting neurons, but this is less likely to be so for V2 and MT. J. Comp. Neurol. 425:345–368, 2000. © 2000 Wiley‐Liss, Inc.

[1]  R Gattass,et al.  Cortical afferents of visual area MT in the Cebus monkey: Possible homologies between New and old World monkeys , 1993, Visual Neuroscience.

[2]  Keiji Tanaka,et al.  Divergent backward projections from the anterior part of the inferotemporal cortex (area TE) in the macaque , 2000, The Journal of comparative neurology.

[3]  S. Zeki,et al.  Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex , 1985, Nature.

[4]  A. Burkhalter,et al.  Role of GABAB receptor-mediated inhibition in reciprocal interareal pathways of rat visual cortex. , 1999, Journal of neurophysiology.

[5]  C. Gross Contribution of striate cortex and the superior colliculus to visual function in area MT, the superior temporal polysensory area and inferior temporal cortex , 1991, Neuropsychologia.

[6]  P A Salin,et al.  Response selectivity of neurons in area MT of the macaque monkey during reversible inactivation of area V1. , 1992, Journal of neurophysiology.

[7]  J. M. Hupé,et al.  Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons , 1998, Nature.

[8]  J. Tigges,et al.  Areal and laminar distribution of neurons interconnecting the central visual cortical areas 17, 18, 19, and MT in squirrel monkey (Saimiri) , 1981, The Journal of comparative neurology.

[9]  K. Rockland The Organization of Feedback Connections from Area V2 (18) to V1 (17) , 1994 .

[10]  J. Kaas,et al.  Cortical connections of area 18 and dorsolateral visual cortex in squirrel monkeys , 1988, Visual Neuroscience.

[11]  M. Nicolelis,et al.  Immediate thalamic sensory plasticity depends on corticothalamic feedback. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[12]  C. Gross,et al.  Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  P Girard,et al.  Feedback connections act on the early part of the responses in monkey visual cortex. , 2001, Journal of neurophysiology.

[14]  D A Pollen,et al.  On the neural correlates of visual perception. , 1999, Cerebral cortex.

[15]  J. Kaas,et al.  Cortical integration of parallel pathways in the visual system of primates , 1989, Brain Research.

[16]  K. Rockland,et al.  Collateralized divergent feedback connections that target multiple cortical areas , 1996, The Journal of comparative neurology.

[17]  Andreas Burkhalter,et al.  Microcircuitry of forward and feedback connections within rat visual cortex , 1996, The Journal of comparative neurology.

[18]  R K Carder,et al.  Neurochemical compartmentation of monkey and human visual cortex: Similarities and variations in calbindin immunoreactivity across species , 1993, Visual Neuroscience.

[19]  S. Grossberg,et al.  Contrast-sensitive perceptual grouping and object-based attention in the laminar circuits of primary visual cortex , 2000, Vision Research.

[20]  Leslie G. Ungerleider,et al.  Neurofilament protein is differentially distributed in subpopulations of corticocortical projection neurons in the macaque monkey visual pathways , 1996, The Journal of comparative neurology.

[21]  H. Kennedy,et al.  Laminar Distribution of Neurons in Extrastriate Areas Projecting to Visual Areas V1 and V4 Correlates with the Hierarchical Rank and Indicates the Operation of a Distance Rule , 2000, The Journal of Neuroscience.

[22]  R E Weller,et al.  Cortical connections of the caudal subdivision of the dorsolateral area (V4) in monkeys , 1991, The Journal of comparative neurology.

[23]  A S Feng,et al.  Temporal coding in the frog auditory midbrain: the influence of duration and rise-fall time on the processing of complex amplitude-modulated stimuli. , 1992, Journal of neurophysiology.

[24]  P A Salin,et al.  Corticocortical connections in the visual system: structure and function. , 1995, Physiological reviews.

[25]  K. Rockland,et al.  Single axon analysis of pulvinocortical connections to several visual areas in the Macaque , 1999, The Journal of comparative neurology.

[26]  A. Reiner,et al.  Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies , 1992, Journal of Neuroscience Methods.

[27]  B. Lia,et al.  Distribution of neurons projecting to the superior colliculus correlates with thick cytochrome oxidase stripes in macaque visual area V2 , 1997, The Journal of comparative neurology.

[28]  Kathleen S. Rockland,et al.  Elements of Cortical Architecture , 1997 .

[29]  K. Rockland,et al.  Morphology of individual axons projecting from area V2 to MT in the macaque , 1995, The Journal of comparative neurology.

[30]  H. Kennedy,et al.  A double-labeling investigation of the afferent connectivity to cortical areas V1 and V2 of the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  A. Vania Apkarian,et al.  Biotin-dextran: a sensitive anterograde tracer for neuroanatomic studies in rat and monkey , 1992, Journal of Neuroscience Methods.

[32]  S. Zeki,et al.  The Organization of Connections between Areas V5 and V2 in Macaque Monkey Visual Cortex , 1989, The European journal of neuroscience.

[33]  K. Rockland,et al.  Cortical connections of the occipital lobe in the rhesus monkey: Interconnections between areas 17, 18, 19 and the superior temporal sulcus , 1981, Brain Research.

[34]  G. Blasdel,et al.  Termination of afferent axons in macaque striate cortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  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.

[36]  Jean Bullier,et al.  The Role of Area 17 in the Transfer of Information to Extrastriate Visual Cortex , 1994 .

[37]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[39]  J. Lund,et al.  Anatomical organization of primate visual cortex area VII , 1981, The Journal of comparative neurology.

[40]  K. Rockland,et al.  Divergent cortical connections to entorhinal cortex from area TF in the macaque , 1997, The Journal of comparative neurology.

[41]  S. Zeki,et al.  The Organization of Connections between Areas V5 and V1 in Macaque Monkey Visual Cortex , 1989, The European journal of neuroscience.

[42]  J. Kaas,et al.  Cortical connections of the dorsomedial visual area in new world owl monkeys (Aotus trivirgatus) and squirrel monkeys (Saimiri sciureus) , 1998, The Journal of comparative neurology.

[43]  J. T. Weber,et al.  Chemoarchitectonic subdivisions of the visual pulvinar in monkeys and their connectional relations with the middle temporal and rostral dorsolateral visual areas, MT and DLr , 1993, The Journal of comparative neurology.

[44]  Leslie G. Ungerleider,et al.  Cortical connections of visual area MT in the macaque , 1986, The Journal of comparative neurology.

[45]  K. Rockland,et al.  Bistratified distribution of terminal arbors of individual axons projecting from area V1 to middle temporal area (MT) in the macaque monkey , 1989, Visual Neuroscience.

[46]  L A Krubitzer,et al.  Cortical connections of MT in four species of primates: Areal, modular, and retinotopic patterns , 1990, Visual Neuroscience.

[47]  J. Kaas,et al.  Retinotopic patterns of connections of area 17 with visual areas V‐II and MT in macaque monkeys , 1983, The Journal of comparative neurology.

[48]  K. Rockland,et al.  Terminal arbors of individual “Feedback” axons projecting from area V2 to V1 in the macaque monkey: A study using immunohistochemistry of anterogradely transported Phaseolus vulgaris‐leucoagglutinin , 1989, The Journal of comparative neurology.

[49]  V. Casagrande,et al.  Relationships between cytochrome oxidase (CO) blobs in primate primary visual cortex (V1) and the distribution of neurons projecting to the middle temporal area (MT) , 1999, The Journal of comparative neurology.

[50]  J. C. Anderson,et al.  The Connection from Cortical Area V1 to V5: A Light and Electron Microscopic Study , 1998, The Journal of Neuroscience.

[51]  J. Kaas,et al.  Is most of neural plasticity in the thalamus cortical? , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[52]  K. Rockland,et al.  Divergent feedback connections from areas V4 and TEO in the macaque , 1994, Visual Neuroscience.