Distinct Mechanisms for Top-Down Control of Neural Gain and Sensitivity in the Owl Optic Tectum

We demonstrate that distinct mechanisms of top-down control regulate, respectively, the sensitivity and gain of sensory responses in the owl's optic tectum (OT). Electrical microstimulation in the forebrain gaze control area, the arcopallial gaze field (AGF), results in a space-specific regulation of sensory responses in the OT. AGF microstimulation increases the responsiveness of OT neurons representing stimuli at the same location as that represented at the AGF site. We show that the mechanism that underlies this effect operates focally to enhance neuronal sensitivity and improve tuning consistency and spatial resolution. At the same time, AGF microstimulation decreases the responsiveness of OT neurons representing stimuli at all other locations. The mechanism that underlies this effect operates globally to modulate neuronal gain. The coordinated action of these different mechanisms can account for many of the reported effects of spatial attention on neural responses in monkeys and on behavioral performance in humans.

[1]  H. Spitzer,et al.  Increased attention enhances both behavioral and neuronal performance. , 1988, Science.

[2]  Eric I. Knudsen,et al.  Top-Down Control of Multimodal Sensitivity in the Barn Owl Optic Tectum , 2007, The Journal of Neuroscience.

[3]  H. Karten,et al.  Columnar projections from the cholinergic nucleus isthmi to the optic tectum in chicks (Gallus gallus): A possible substrate for synchronizing tectal channels , 2006, The Journal of comparative neurology.

[4]  J. Letelier,et al.  A Cholinergic Gating Mechanism Controlled by Competitive Interactions in the Optic Tectum of the Pigeon , 2007, The Journal of Neuroscience.

[5]  A. Burkhalter,et al.  Organization of long-range inhibitory connections with rat visual cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  Eric I. Knudsen,et al.  Top-down gain control of the auditory space map by gaze control circuitry in the barn owl , 2006, Nature.

[7]  B. C. Motter.  Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. , 1993, Journal of neurophysiology.

[8]  B. Sakitt.  Indices of Discriminability , 1973, Nature.

[9]  Mikko Sams,et al.  Selective Attention Increases Both Gain and Feature Selectivity of the Human Auditory Cortex , 2007, PloS one.

[10]  Terry T. Takahashi,et al.  Prediction of auditory spatial acuity from neural images on the owl's auditory space map , 2003, Nature.

[11]  L. Swanson,et al.  Immunohistochemical localization of neuronal nicotinic receptors in the rodent central nervous system , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  J. Hoffman,et al.  The role of visual attention in saccadic eye movements , 1995, Perception & psychophysics.

[13]  S. Treue,et al.  Attentional Modulation Strength in Cortical Area MT Depends on Stimulus Contrast , 2002, Neuron.

[14]  R. Desimone,et al.  Attention Increases Sensitivity of V4 Neurons , 2000, Neuron.

[15]  Katherine M. Armstrong,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2003, Nature.

[16]  E. Knudsen.  Fundamental components of attention. , 2007, Annual review of neuroscience.

[17]  Y. Yanagawa,et al.  Nicotinic acetylcholine receptor subtypes involved in facilitation of GABAergic inhibition in mouse superficial superior colliculus. , 2005, Journal of neurophysiology.

[18]  Avinash D. S. Bala,et al.  Auditory Spatial Acuity Approximates the Resolving Power of Space-Specific Neurons , 2007, PloS one.

[19]  C. Koch,et al.  Computational modelling of visual attention , 2001, Nature Reviews Neuroscience.

[20]  E I Knudsen,et al.  Neural maps of interaural time and intensity differences in the optic tectum of the barn owl , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  Katherine M. Armstrong,et al.  Visuomotor Origins of Covert Spatial Attention , 2003, Neuron.

[22]  J. Maunsell,et al.  The role of attention in visual processing. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[23]  Tirin Moore,et al.  Changes in Visual Receptive Fields with Microstimulation of Frontal Cortex , 2006, Neuron.

[24]  M. Hawken,et al.  Gain Modulation by Nicotine in Macaque V1 , 2007, Neuron.

[25]  James R Müller,et al.  Microstimulation of the superior colliculus focuses attention without moving the eyes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[26]  H. Karten,et al.  Morphology and connections of nucleus isthmi pars magnocellularis in chicks (Gallus gallus) , 2004, The Journal of comparative neurology.

[27]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[28]  M. Segraves,et al.  Muscimol-induced inactivation of monkey frontal eye field: effects on visually and memory-guided saccades. , 1999, Journal of neurophysiology.

[29]  The effects of nicotinic and muscarinic receptor activation on patch-clamped cells in the optic tectum of rana pipiens , 2003, Neuroscience.

[30]  J. Maunsell,et al.  Effects of spatial attention on contrast response functions in macaque area V4. , 2006, Journal of neurophysiology.

[31]  M. Carrasco,et al.  Attention enhances contrast sensitivity at cued and impairs it at uncued locations , 2005, Vision Research.

[32]  J. Lindstrom,et al.  Nicotinic acetylcholine receptor-like molecules in the retina, retinotectal pathway, and optic tectum of the frog , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  R. Desimone,et al.  Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4 , 1999, The Journal of Neuroscience.

[34]  Xiao-Jing Wang,et al.  An Integrated Microcircuit Model of Attentional Processing in the Neocortex , 2007, The Journal of Neuroscience.

[35]  Marisa Carrasco,et al.  Attention improves or impairs visual performance by enhancing spatial resolution , 1998, Nature.

[36]  Robert M. McPeek,et al.  Deficits in saccade target selection after inactivation of superior colliculus , 2004, Nature Neuroscience.

[37]  C. Koch,et al.  Spatial vision thresholds in the near absence of attention , 1997, Vision Research.

[38]  D. G. Albrecht,et al.  Striate cortex of monkey and cat: contrast response function. , 1982, Journal of neurophysiology.

[39]  J. Maunsell,et al.  Feature-based attention in visual cortex , 2006, Trends in Neurosciences.

[40]  E. Niebur,et al.  Growth patterns in the developing brain detected by using continuum mechanical tensor maps , 2022 .

[41]  M. Sarter,et al.  Cognitive functions of cortical acetylcholine: toward a unifying hypothesis , 1997, Brain Research Reviews.

[42]  E I Knudsen,et al.  Characterization of a forebrain gaze field in the archistriatum of the barn owl: microstimulation and anatomical connections , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  S. David,et al.  Auditory attention : focusing the searchlight on sound , 2007 .

[44]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[45]  E I Knudsen,et al.  Binaural tuning of auditory units in the forebrain archistriatal gaze fields of the barn owl: local organization but no space map , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  H. Cline,et al.  Light-induced calcium influx into retinal axons is regulated by presynaptic nicotinic acetylcholine receptor activity in vivo. , 1999, Journal of neurophysiology.

[47]  H. Karten,et al.  Distribution, laminar location, and morphology of tectal neurons projecting to the isthmo‐optic nucleus and the nucleus isthmi, pars parvocellularis in the pigeon (Columba livia) and chick (Gallus domesticus): A retrograde labelling study , 1991, The Journal of comparative neurology.

[48]  Michael E. Hasselmo,et al.  Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection , 2005, Brain Research Reviews.

[49]  T Moore,et al.  Control of eye movements and spatial attention. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[50]  The Role of Attention in Visual Processing , 1991 .

[51]  H Zeier,et al.  The archistriatum of the pigeon: organization of afferent and efferent connections. , 1971, Brain research.

[52]  A. Reiner,et al.  Distribution of choline acetyltransferase immunoreactivity in the pigeon brain , 1994, The Journal of comparative neurology.

[53]  J. Reynolds,et al.  Attentional modulation of visual processing. , 2004, Annual review of neuroscience.

[54]  Tirin Moore,et al.  Rapid enhancement of visual cortical response discriminability by microstimulation of the frontal eye field , 2007, Proceedings of the National Academy of Sciences.

[55]  Louise S. Delicato,et al.  Acetylcholine contributes through muscarinic receptors to attentional modulation in V1 , 2008, Nature.

[56]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[57]  Eric I. Knudsen,et al.  Auditory and Visual Space Maps in the Cholinergic Nucleus Isthmi Pars Parvocellularis of the Barn Owl , 2006, The Journal of Neuroscience.

[58]  R. Oostenveld,et al.  Tactile Spatial Attention Enhances Gamma-Band Activity in Somatosensory Cortex and Reduces Low-Frequency Activity in Parieto-Occipital Areas , 2006, The Journal of Neuroscience.

[59]  J. Findlay,et al.  The Relationship between Eye Movements and Spatial Attention , 1986, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[60]  M. Sarter,et al.  Glutamatergic Contributions to Nicotinic Acetylcholine Receptor Agonist-Evoked Cholinergic Transients in the Prefrontal Cortex , 2008, The Journal of Neuroscience.

[61]  T. Womelsdorf,et al.  Dynamic shifts of visual receptive fields in cortical area MT by spatial attention , 2006, Nature Neuroscience.

[62]  T. Moore,et al.  Microstimulation of the frontal eye field and its effects on covert spatial attention. , 2004, Journal of neurophysiology.

[63]  M. Cynader,et al.  [3H]nicotine binding sites are associated with mammalian optic nerve terminals , 1988, Visual Neuroscience.

[64]  E. Knudsen,et al.  Disruption of auditory spatial working memory by inactivation of the forebrain archistriatum in barn owls , 1996, Nature.