Lesions of prefrontal cortex reduce attentional modulation of neuronal responses and synchrony in V4

It is widely held that the frontal eye field (FEF) in prefrontal cortex (PFC) modulates processing in visual cortex with attention, although the evidence that it is necessary is equivocal. To help identify critical sources of attentional feedback to area V4, we surgically removed the entire lateral PFC, including the FEF, in one hemisphere and transected the corpus callosum and anterior commissure in two macaques. This deprived V4 of PFC input in one hemisphere while keeping the other hemisphere intact. In the absence of PFC, attentional effects on neuronal responses and synchrony in V4 were substantially reduced and the remaining effects of attention were delayed in time, indicating a critical role for PFC. Conversely, distracters captured attention and influenced V4 responses. However, because the effects of attention in V4 were not eliminated by PFC lesions, other sources of top-down attentional control signals to visual cortex must exist outside of PFC.

[1]  Alexandre Zénon,et al.  Attention deficits without cortical neuronal deficits , 2012, Nature.

[2]  A. Thiele,et al.  Comparison of spatial integration and surround suppression characteristics in spiking activity and the local field potential in macaque V1 , 2008, The European journal of neuroscience.

[3]  R. Desimone,et al.  Long-range neural coupling through synchronization with attention. , 2009, Progress in brain research.

[4]  J. Duncan,et al.  Filtering of neural signals by focused attention in the monkey prefrontal cortex , 2002, Nature Neuroscience.

[5]  R. Desimone,et al.  Gamma-band synchronization in visual cortex predicts speed of change detection , 2006, Nature.

[6]  Stephen J. Gotts,et al.  Cell-Type-Specific Synchronization of Neural Activity in FEF with V4 during Attention , 2012, Neuron.

[7]  P. Fries.  A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[8]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

[9]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

[10]  Kenneth M. Heilman,et al.  Frontal lobe neglect in man , 1972, Neurology.

[11]  Anna C Nobre,et al.  FEF TMS affects visual cortical activity. , 2006, Cerebral cortex.

[12]  R. M. Siegel,et al.  Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule , 1990, The Journal of comparative neurology.

[13]  Leslie G. Ungerleider,et al.  Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. , 1994, Cerebral cortex.

[14]  Taihei Ninomiya,et al.  Segregated Pathways Carrying Frontally Derived Top-Down Signals to Visual Areas MT and V4 in Macaques , 2012, The Journal of Neuroscience.

[15]  R. Knight,et al.  Human prefrontal lesions increase distractibility to irrelevant sensory inputs , 1995, Neuroreport.

[16]  Stephen J. Gotts,et al.  Cell-Type-Specific Synchronization of Neural Activity in FEF with V 4 during Attention , 2022 .

[17]  J. Maunsell,et al.  Attention improves performance primarily by reducing interneuronal correlations , 2009, Nature Neuroscience.

[18]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[19]  H. Barbas,et al.  The laminar pattern of connections between prefrontal and anterior temporal cortices in the Rhesus monkey is related to cortical structure and function. , 2000, Cerebral cortex.

[20]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[21]  D. Pandya,et al.  The cortical connectivity of the prefrontal cortex in the monkey brain , 2012, Cortex.

[22]  Y. Saalmann,et al.  The Pulvinar Regulates Information Transmission Between Cortical Areas Based on Attention Demands , 2012, Science.

[23]  R. Knight,et al.  Prefrontal modulation of visual processing in humans , 2000, Nature Neuroscience.

[24]  Theodore P. Zanto,et al.  Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory , 2011, Nature Neuroscience.

[25]  Robert Desimone,et al.  Cortical Connections of Area V4 in the Macaque , 2008 .

[26]  S. Shipp.  The brain circuitry of attention , 2004, Trends in Cognitive Sciences.

[27]  Etienne Olivier,et al.  A Deficit in Covert Attention after Parietal Cortex Inactivation in the Monkey , 2004, Neuron.

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

[29]  Junying Yuan,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2022 .

[30]  Robert Desimone,et al.  Cortical connections of area V4 in the macaque. , 2000, Cerebral cortex.

[31]  M. Mesulam.  A cortical network for directed attention and unilateral neglect , 1981, Annals of neurology.

[32]  T. Moore,et al.  CONTROL OF VISUAL CORTICAL SIGNALS BY PREFRONTAL DOPAMINE , 2011, Nature.

[33]  N. P. Bichot,et al.  Dissociation of visual discrimination from saccade programming in macaque frontal eye field. , 1997, Journal of neurophysiology.

[34]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[35]  Robert Desimone,et al.  Top–Down Attentional Deficits in Macaques with Lesions of Lateral Prefrontal Cortex , 2007, The Journal of Neuroscience.

[36]  J. Duncan.  Disorganisation of behaviour after frontal lobe damage , 1986 .

[37]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[38]  M. Merzenich,et al.  Reorganization of neocortical representations after brain injury: a neurophysiological model of the bases of recovery from stroke. , 1987, Progress in brain research.

[39]  Partha P. Mitra,et al.  Sampling Properties of the Spectrum and Coherency of Sequences of Action Potentials , 2000, Neural Computation.

[40]  Ivan N Pigarev,et al.  Neural Mechanisms of Visual Attention: How Top-Down Feedback Highlights Relevant Locations , 2007, Science.

[41]  J. Maunsell,et al.  Differences in Gamma Frequencies across Visual Cortex Restrict Their Possible Use in Computation , 2010, Neuron.

[42]  P. Roelfsema,et al.  Bottom-Up Dependent Gating of Frontal Signals in Early Visual Cortex , 2008, Science.

[43]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[44]  J. Gottlieb,et al.  Distinct neural mechanisms of distractor suppression in the frontal and parietal lobe , 2012, Nature Neuroscience.

[45]  S. Petersen,et al.  Pulvinar nuclei of the behaving rhesus monkey: visual responses and their modulation. , 1985, Journal of neurophysiology.

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

[47]  W. Freiwald,et al.  Coherent oscillatory activity in monkey area v4 predicts successful allocation of attention. , 2005, Cerebral cortex.

[48]  N. Huang,et al.  The empirical mode decomposition and the Hilbert spectrum for nonlinear and non-stationary time series analysis , 1998, Proceedings of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[49]  R. Desimone,et al.  The Effects of Visual Stimulation and Selective Visual Attention on Rhythmic Neuronal Synchronization in Macaque Area V4 , 2008, The Journal of Neuroscience.

[50]  Jude F. Mitchell,et al.  Spatial Attention Decorrelates Intrinsic Activity Fluctuations in Macaque Area V4 , 2009, Neuron.

[51]  Ehud Zohary,et al.  Correlated neuronal discharge rate and its implications for psychophysical performance , 1994, Nature.

[52]  Robert Desimone,et al.  Parallel and Serial Neural Mechanisms for Visual Search in Macaque Area V4 , 2005, Science.

[53]  R. Marrocco,et al.  Electrical microstimulation of primate posterior parietal cortex initiates orienting and alerting components of covert attention , 2002, Experimental Brain Research.

[54]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[55]  Robert Desimone,et al.  Subcortical connections of area V4 in the macaque , 2000, The Journal of comparative neurology.