Functional streams in occipito-frontal connections in the monkey

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Abstract

It is known that the prestriate cortical regions that project to area LIP in parietal cortex and to areas TEO and TE in temporal cortex are mostly separated. Two separate streams of information transfer from occipital cortex can thus be distinguished. We wished to determine whether the parietal and temporal streams remain segregated in their projections to frontal cortex. Paired injections of retrograde fluorescent tracers were placed in parietal and temporal cortex, or in the lateral and medial parts of the frontal eye field (FEF). The cortical regions containing retrogradely labeled cells were reconstructed in two-dimensional maps. The results show that temporal cortex mainly projects to lateral FEF (area 45). Parietal cortex sends projections to medial FEF (area 8a) and to lateral FEF, as well as to area 46. Thus, the parietal and temporal streams converge in lateral FEF. Most of the occipital regions projecting to medial FEF are the same as those projecting to parietal cortex, whereas lateral FEF receives afferents from the same occipital regions as those sending projections to temporal cortex. Thus, one can distinguish two interconnected networks. One is associated with the inferotemporal cortex and includes areas of the ventral bank and fundus of the superior temporal sulcus (STS), lateral FEF and ventral prestriate cortex. This network emphasizes central vision, small saccades and form recognition. The other network is linked to cortex of the intraparietal sulcus. It consists of areas of the upper bank and fundus of STS, medial FEF and dorsal prestriate cortex. These areas encode peripheral visual field and are active during large saccades.

References (73)

  • S. Barash et al.

    Saccade-related activity in the lateral intraparietal area I. Temporal properties; comparison with area 7a

    J. Neurophysiol.

    (1991)
  • S. Barash et al.

    Saccade-related activity in the lateral intraparietal area II. Spatial properties

    J. Neurophysiol.

    (1991)
  • H. Barbas et al.

    Organization of afferent input to subdivisions of area 8 in the rhesus monkey

    J. Comp. Neurol.

    (1981)
  • G.C. Baylis et al.

    Functional subdivisions of the temporal lobe neocortex

    J. Neurosci.

    (1987)
  • G.J. Blatt et al.

    Visual receptive field organization and cortico-cortical connections of the lateral intraparietal area (area LIP) in the macaque

    J. Comp. Neurol.

    (1990)
  • C.J. Bruce et al.

    Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements

    J. Neurophysiol.

    (1985)
  • C.J. Bruce

    Integration of sensory and motor signals for saccadic eye movements in the primate frontal eye fields

  • D.D. Burman et al.

    Primate frontal eye field activity during natural scanning eye movements

    J. Neurophysiol.

    (1994)
  • M.C. Bushnell et al.

    Behavioral enhancement of visual responses in monkey cerebral cortex I Modulation in posterior parietal cortex related to selective visual attention

    J. Neurophysiol.

    (1981)
  • R.H.S. Carpenter

    The visual origins of ocular motility

    Cronly-Dillon J, ed. Vision and Visual...
  • C. Cavada et al.

    Posterior parietal cortex in rhesus monkey: 11. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe

    J. Comp. Neurol.

    (1989)
  • L. Chelazzi et al.

    A neural basis for visual search in inferior temporal cortex

    Nature

    (1993)
  • C.L. Colby et al.

    The analysis of visual space by the lateral intraperietal area of the monkey: the role of extraretinal signals

  • C. Distler et al.

    Cortical connections of inferior temporal area TEO in macaque monkeys

    J. Comp. Neurol.

    (1993)
  • C.J. Duffy et al.

    Sensitivity of MST neurons to optic flow stimuli. 1. A continuum of response selectivity to large-field stimuli

    J. Neurophysiol.

    (1991)
  • J.-R. Duhamel et al.

    The updating of the representation of visual space in parietal cortex by intended eye movements

    Science

    (1992)
  • M.R. Dursteler et al.

    Pursuit and optokinetic deficits following chemical lesions of cortical areas MT and MST

    J. Neurosci.

    (1988)
  • D.J. Felleman et al.

    Distributed hierarchical processing in the primate cerebral cortex

    Cereb. Cortex

    (1991)
  • R.S. Gellman et al.

    Motion processing for saccadic eye movements in humans

    Exp. Brain Res.

    (1991)
  • J.J. Gibson

    The Perception of the Visual World

    (1950)
  • M.E. Goldberg et al.

    Visual and frontal corticles

  • M.A. Goodale et al.

    Separate visual pathways for perception and action

    Trends in Neuroscience

    (1992)
  • C.F. Keating et al.

    Monkeys and mug shots: Cues used by rbesus monkeys (Macaca mulatta) to recognize a human face

    J. Comp. Psychol.

    (1993)
  • Keating

    Frontal eye field lesions impair predictive and visuallyguided pursuit eye movements

    Exp. Brain Res.

    (1991)
  • H. Komatsu et al.

    Relation of cortical areas MT and MST to pursuit eye movements. 1. Localization and visual properties of neurons

    J. Neurophysiol.

    (1988)
  • H. Komatsu et al.

    Modulation of pursuit eye movements by stimulation of cortical areas MT and MST

    J. Neurophysiol.

    (1989)

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