Dynamic Construction of a Coherent Attentional State in a Prefrontal Cell Population

Summary Prefrontal cortex has been proposed to show highly adaptive information coding, with neurons dynamically allocated to processing task-relevant information. To track this dynamic allocation in monkey prefrontal cortex, we used time-resolved measures of neural population activity in a simple case of competition between target (behaviorally critical) and nontarget objects in opposite visual hemifields. Early in processing, there were parallel responses to competing inputs, with neurons in each hemisphere dominated by the contralateral stimulus. Later, the nontarget lost control of neural activity, with emerging global control by the behaviorally critical target. The speed of transition reflected the competitive weights of different display elements, occurring most rapidly when relative behavioral significance was well established by training history. In line with adaptive coding, the results show widespread reallocation of prefrontal processing resources as an attentional focus is established.

[1]  E. Miller,et al.  Serial, Covert Shifts of Attention during Visual Search Are Reflected by the Frontal Eye Fields and Correlated with Population Oscillations , 2009, Neuron.

[2]  H Pashler,et al.  Dual-task interference and the cerebral hemispheres. , 1993, Journal of experimental psychology. Human perception and performance.

[3]  M. Botvinick,et al.  Conflict monitoring and cognitive control. , 2001, Psychological review.

[4]  C. Bundesen,et al.  Parallel processing in a multifeature whole-report paradigm. , 2007, Journal of experimental psychology. Human perception and performance.

[5]  Markus Siegel,et al.  Neural substrates of cognitive capacity limitations , 2011, Proceedings of the National Academy of Sciences.

[6]  N. P. Bichot,et al.  Visual feature selectivity in frontal eye fields induced by experience in mature macaques , 1996, Nature.

[7]  D. Norman,et al.  Attention to Action: Willed and Automatic Control of Behavior Technical Report No. 8006. , 1980 .

[8]  Leslie G. Ungerleider,et al.  Projections from inferior temporal cortex to prefrontal cortex via the uncinate fascicle in rhesus monkeys , 2004, Experimental Brain Research.

[9]  D. Pandya,et al.  Comparison of prefrontal architecture and connections. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[10]  M. Kerszberg,et al.  A Neuronal Model of a Global Workspace in Effortful Cognitive Tasks , 2001 .

[11]  C. Bundesen,et al.  A neural theory of visual attention: bridging cognition and neurophysiology. , 2005, Psychological review.

[12]  Peter W Dicke,et al.  Neuron-specific contribution of the superior colliculus to overt and covert shifts of attention , 2004, Nature Neuroscience.

[13]  Stefan Everling,et al.  Specific Contributions of Ventromedial, Anterior Cingulate, and Lateral Prefrontal Cortex for Attentional Selection and Stimulus Valuation , 2011, PLoS biology.

[14]  John Duncan,et al.  Detection of Fixed and Variable Targets in the Monkey Prefrontal Cortex , 2009, Cerebral cortex.

[15]  D. Heeger,et al.  The Normalization Model of Attention , 2009, Neuron.

[16]  N. Sigala,et al.  Dynamic Coding for Cognitive Control in Prefrontal Cortex , 2013, Neuron.

[17]  J. Martinez-Trujillo,et al.  Strength of Response Suppression to Distracter Stimuli Determines Attentional-Filtering Performance in Primate Prefrontal Neurons , 2011, Neuron.

[18]  A. D. Fisk,et al.  Degree of consistent training: Improvements in search performance and automatic process development , 1982, Perception & psychophysics.

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

[20]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[21]  D. Broadbent Perception and communication , 1958 .

[22]  R. Shiffrin,et al.  Controlled and automatic human information processing: I , 1977 .

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

[24]  R. Desimone,et al.  Responses of Neurons in Inferior Temporal Cortex during Memory- Guided Visual Search , 1998 .

[25]  Earl K. Miller,et al.  Selective representation of relevant information by neurons in the primate prefrontal cortex , 1998, Nature.

[26]  H. Egeth,et al.  Parallel versus serial processing in visual search: further evidence from subadditive effects of visual quality. , 1991 .

[27]  Patrick Bourke,et al.  A General Factor Involved in Dual-task Performance Decrement , 1996 .

[28]  J. Duncan An adaptive coding model of neural function in prefrontal cortex , 2001 .

[29]  Joonyeol Lee,et al.  Attentional Modulation of MT Neurons with Single or Multiple Stimuli in Their Receptive Fields , 2010, The Journal of Neuroscience.

[30]  J. Schall,et al.  Saccade target selection in frontal eye field of macaque. I. Visual and premovement activation , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

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

[33]  Chris J. Tinsley,et al.  Selective representation of task‐relevant objects and locations in the monkey prefrontal cortex , 2006, The European journal of neuroscience.

[34]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[35]  Y. Miyashita,et al.  Top-down signal from prefrontal cortex in executive control of memory retrieval , 1999, Nature.

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

[37]  Earl K. Miller,et al.  Cognitive focus through adaptive neural coding in the primate prefrontal cortex , 2002 .

[38]  N. P. Bichot,et al.  Effects of similarity and history on neural mechanisms of visual selection , 1999, Nature Neuroscience.

[39]  P. Cavanagh,et al.  Independent Resources for Attentional Tracking in the Left and Right Visual Hemifields , 2005, Psychological science.

[40]  J. B. Levitt,et al.  Patterns of intrinsic and associational circuitry in monkey prefrontal cortex , 1996, The Journal of comparative neurology.

[41]  Eric L. Denovellis,et al.  Synchronous Oscillatory Neural Ensembles for Rules in the Prefrontal Cortex , 2012, Neuron.

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

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

[44]  John Duncan,et al.  Target Detection by Opponent Coding in Monkey Prefrontal Cortex , 2010, Journal of Cognitive Neuroscience.

[45]  D. Kahneman Attention and Effort , 1973 .

[46]  Pieter R. Roelfsema,et al.  Object-based attention in the primary visual cortex of the macaque monkey , 1998, Nature.

[47]  M. Pinsk,et al.  Attention modulates responses in the human lateral geniculate nucleus , 2002, Nature Neuroscience.

[48]  R. Marois,et al.  Capacity limits of information processing in the brain , 2005, Trends in Cognitive Sciences.