Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons

A single visual stimulus activates neurons in many different cortical areas. A major challenge in cortical physiology is to understand how the neural activity in these numerous active zones leads to a unified percept of the visual scene. The anatomical basis for these interactions is the dense network of connections that link the visual areas. Within this network, feedforward connections transmit signals from lower-order areas such as V1 or V2 to higher-order areas. In addition, there is a dense web of feedback connections which, despite their anatomical prominence, remain functionally mysterious. Here we show, using reversible inactivation of a higher-order area (monkey area V5/MT), that feedback connections serve to amplify and focus activity of neurons in lower-order areas, and that they are important in the differentiation of figure from ground, particularly in the case of stimuli of low visibility. More specifically, we show that feedback connections facilitate responses to objects moving within the classical receptive field; enhance suppression evoked by background stimuli in the surrounding region; and have the strongest effects for stimuli of low salience.

[1]  Robert Tibshirani,et al.  An Introduction to the Bootstrap , 1994 .

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

[3]  P. Viviani,et al.  The law relating the kinematic and figural aspects of drawing movements. , 1983, Acta psychologica.

[4]  C. Li,et al.  Extensive integration field beyond the classical receptive field of cat's striate cortical neurons--classification and tuning properties. , 1994, Vision research.

[5]  Paul Antoine Salin,et al.  Visuotopic organization of corticocortical connections in the visual system of the cat , 1992, The Journal of comparative neurology.

[6]  E. Bizzi,et al.  Consolidation in human motor memory , 1996, Nature.

[7]  H. Kennedy,et al.  Topography of the afferent connectivity of area 17 in the macaque monkey: A double‐labelling study , 1986, The Journal of comparative neurology.

[8]  Michael I. Jordan,et al.  An internal model for sensorimotor integration. , 1995, Science.

[9]  M. Mignard,et al.  Paths of information flow through visual cortex. , 1991, Science.

[10]  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.

[11]  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.

[12]  P. Fitts The information capacity of the human motor system in controlling the amplitude of movement. , 1954, Journal of experimental psychology.

[13]  S G Lomber,et al.  Learning and recall of form discriminations during reversible cooling deactivation of ventral-posterior suprasylvian cortex in the cat. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[14]  C. Harris,et al.  Fourier analysis of saccades in monkeys and humans. , 1990, Journal of neurophysiology.

[15]  C. Harris On the optimal control of behaviour: a stochastic perspective , 1998, Journal of Neuroscience Methods.

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

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

[18]  P. Schiller,et al.  Effect of cooling area 18 on striate cortex cells in the squirrel monkey. , 1982, Journal of neurophysiology.

[19]  W. Andrew The vertebrate visual system , 1957 .

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

[21]  J. B. Levitt,et al.  Contrast dependence of contextual effects in primate visual cortex , 1997, nature.

[22]  S. Gielen,et al.  A quantitative analysis of generation of saccadic eye movements by burst neurons. , 1981, Journal of neurophysiology.

[23]  D. V. van Essen,et al.  Antibody labeling of functional subdivisions in visual cortex: Cat-301 immunoreactivity in striate and extrastriate cortex of the macaque monkey , 1990, Visual Neuroscience.

[24]  D. Wolpert,et al.  Temporal and amplitude generalization in motor learning. , 1998, Journal of neurophysiology.

[25]  P. Viviani,et al.  A developmental study of the relationship between geometry and kinematics in drawing movements. , 1991, Journal of experimental psychology. Human perception and performance.

[26]  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.

[27]  J. Lackner,et al.  Rapid adaptation to Coriolis force perturbations of arm trajectory. , 1994, Journal of neurophysiology.

[28]  G A Orban,et al.  Functional impact of cerebral connections. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[29]  H. Collewijn,et al.  Binocular co‐ordination of human vertical saccadic eye movements. , 1988, The Journal of physiology.

[30]  Kathleen S. Rockland,et al.  Primary Visual Cortex in Primates , 1994, Cerebral Cortex.

[31]  J. Nelson,et al.  Orientation-selective inhibition from beyond the classic visual receptive field , 1978, Brain Research.

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

[33]  H. Clamann Statistical analysis of motor unit firing patterns in a human skeletal muscle. , 1969, Biophysical journal.

[34]  D Goodman,et al.  On the nature of human interlimb coordination. , 1979, Science.

[35]  Vernon B. Brooks,et al.  Study of brain function by local, reversible cooling , 1983 .

[36]  D. J. Felleman,et al.  Cortical connections of areas V3 and VP of macaque monkey extrastriate visual cortex , 1997, The Journal of comparative neurology.

[37]  J. W. Wolfe,et al.  Time-Optimal Control of Saccadic Eye Movements , 1987, IEEE Transactions on Biomedical Engineering.

[38]  T. Flash,et al.  The coordination of arm movements: an experimentally confirmed mathematical model , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  J. Bullier,et al.  Visual latencies in areas V1 and V2 of the macaque monkey , 1995, Visual Neuroscience.

[40]  D. Wolpert Computational approaches to motor control , 1997, Trends in Cognitive Sciences.

[41]  R A Abrams,et al.  Optimality in human motor performance: ideal control of rapid aimed movements. , 1988, Psychological review.

[42]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  W. Merigan,et al.  Motion perception following lesions of the superior temporal sulcus in the monkey. , 1994, Cerebral cortex.

[44]  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.

[45]  P. Matthews Relationship of firing intervals of human motor units to the trajectory of post‐spike after‐hyperpolarization and synaptic noise. , 1996, The Journal of physiology.

[46]  N. Hogan An organizing principle for a class of voluntary movements , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  宇野 洋二,et al.  Formation and control of optimal trajectory in human multijoint arm movement : minimum torque-change model , 1988 .

[48]  F A Mussa-Ivaldi,et al.  Adaptive representation of dynamics during learning of a motor task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  H. Condé,et al.  Effects of local cooling upon conduction and synaptic transmission. , 1972, Brain research.

[50]  C. Harris,et al.  Does saccadic undershoot minimize saccadic flight-time? A Monte-Carlo study , 1995, Vision Research.