Persistent neural activity in the human frontal cortex when maintaining space that is “off the map”

During the maintenance of visuospatial information, neural activity in the frontal eye field (FEF) persists and is thought to be an important neural mechanism for visual working memory. We used functional magnetic resonance imaging to examine whether human FEF activity persists when maintaining auditory space and whether it is selective for retinal versus extra-retinal space. Subjects performed an audiospatial working-memory task using sounds recorded from microphones placed in each subject's ear canals, which preserved the interaural time and level differences that are critical for sound localization. Putative FEF activity persisted when maintaining auditory-cued space, even for locations behind the head to which it is impossible to make saccades. Therefore, human FEF activity represents both retinal and extra-retinal space.

[1]  J D Watson,et al.  Nonparametric Analysis of Statistic Images from Functional Mapping Experiments , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[2]  Clayton E. Curtis,et al.  The effects of prefrontal lesions on working memory performance and theory , 2004, Cognitive, affective & behavioral neuroscience.

[3]  Clayton E Curtis,et al.  Cortical activity time locked to the shift and maintenance of spatial attention. , 2008, Cerebral cortex.

[4]  J. D. Connolly,et al.  Saccade preparation signals in the human frontal and parietal cortices. , 2008, Journal of neurophysiology.

[5]  Donald J. Reichard,et al.  A SELECTIVE REVIEW , 2007 .

[6]  S. Sterbing-D’Angelo,et al.  Behavioral/systems/cognitive Multisensory Space Representations in the Macaque Ventral Intraparietal Area , 2022 .

[7]  Ravi S. Menon,et al.  Comparison of memory- and visually guided saccades using event-related fMRI. , 2004, Journal of neurophysiology.

[8]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[9]  R. Wurtz,et al.  Frontal eye field sends delay activity related to movement, memory, and vision to the superior colliculus. , 2001, Journal of neurophysiology.

[10]  Clayton E Curtis,et al.  Selection and maintenance of saccade goals in the human frontal eye fields. , 2006, Journal of neurophysiology.

[11]  Yale E Cohen,et al.  Motor-related signals in the intraparietal cortex encode locations in a hybrid, rather than eye-centered reference frame. , 2009, Cerebral cortex.

[12]  C. Curtis,et al.  Persistent activity in the prefrontal cortex during working memory , 2003, Trends in Cognitive Sciences.

[13]  R. Andersen,et al.  The role of the posterior parietal cortex in coordinate transformations for visual-motor integration. , 1988, Canadian journal of physiology and pharmacology.

[14]  Albert F Fuchs,et al.  Contribution of the frontal eye field to gaze shifts in the head-unrestrained monkey: effects of microstimulation. , 2007, Journal of neurophysiology.

[15]  G. S. Russo,et al.  Frontal eye field activity preceding aurally guided saccades. , 1994, Journal of neurophysiology.

[16]  M. Goldberg,et al.  Spatial processing in the monkey frontal eye field. II. Memory responses. , 2001, Journal of neurophysiology.

[17]  G. S. Russo,et al.  Effect of eye position within the orbit on electrically elicited saccadic eye movements: a comparison of the macaque monkey's frontal and supplementary eye fields. , 1993, Journal of neurophysiology.

[18]  Brian D Corneil,et al.  Widespread presaccadic recruitment of neck muscles by stimulation of the primate frontal eye fields. , 2007, Journal of neurophysiology.

[19]  R. Andersen,et al.  Models of the Posterior Parietal Cortex Which Perform Multimodal Integration and Represent Space in Several Coordinate Frames , 2000, Journal of Cognitive Neuroscience.

[20]  B M Gaymard,et al.  Errors of memory-guided saccades in humans with lesions of the frontal eye field and the dorsolateral prefrontal cortex. , 1999, Journal of neurophysiology.

[21]  Y. Cohen,et al.  Eye-centered, head-centered, and complex coding of visual and auditory targets in the intraparietal sulcus. , 2005, Journal of neurophysiology.

[22]  Antti Korvenoja,et al.  Processing of auditory and visual location information in the monkey prefrontal cortex , 2007, Experimental Brain Research.

[23]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[24]  R. Andersen,et al.  Spatially tuned auditory responses in area LIP of macaques performing delayed memory saccades to acoustic targets. , 1996, Journal of neurophysiology.

[25]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[26]  R. Andersen,et al.  Eye-centered, head-centered, and intermediate coding of remembered sound locations in area LIP. , 1996, Journal of neurophysiology.

[27]  M. Goldberg,et al.  Spatial processing in the monkey frontal eye field. I. Predictive visual responses. , 1997, Journal of neurophysiology.

[28]  E. J. Tehovnik,et al.  Eye fields in the frontal lobes of primates , 2000, Brain Research Reviews.

[29]  P. Goldman-Rakic,et al.  Dorsolateral prefrontal lesions and oculomotor delayed-response performance: evidence for mnemonic "scotomas" , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  J. Bullier,et al.  Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  T. Paus Location and function of the human frontal eye-field: A selective review , 1996, Neuropsychologia.

[32]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[33]  C. Bruce,et al.  Primate frontal eye fields. I. Single neurons discharging before saccades. , 1985, Journal of neurophysiology.

[34]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[35]  P. Goldman-Rakic,et al.  Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. , 1998, Journal of neurophysiology.

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

[37]  L Longtang Chen,et al.  Head movements evoked by electrical stimulation in the frontal eye field of the monkey: evidence for independent eye and head control. , 2006, Journal of neurophysiology.

[38]  T. Sawaguchi,et al.  Parallel visuospatial and audiospatial working memory processes in the monkey dorsolateral prefrontal cortex , 2000, Nature Neuroscience.

[39]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[40]  M. D’Esposito,et al.  A Trial-Based Experimental Design for fMRI , 1997, NeuroImage.

[41]  Clayton E. Curtis,et al.  Persistent neural activity during the maintenance of spatial position in working memory , 2008, NeuroImage.

[42]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

[43]  J S Hyde,et al.  Contour‐based registration technique to differentiate between task‐activated and head motion‐induced signal variations in fMRI , 1997, Magnetic resonance in medicine.

[44]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[45]  A. Stevens,et al.  Orienting auditory spatial attention engages frontal eye fields and medial occipital cortex in congenitally blind humans , 2007, Neuropsychologia.

[46]  B. Gaymard,et al.  Eye movement disorders after frontal eye field lesions in humans , 2004, Experimental Brain Research.

[47]  C. Bruce,et al.  Primate frontal eye fields. III. Maintenance of a spatially accurate saccade signal. , 1990, Journal of neurophysiology.

[48]  J F Soechting,et al.  Moving in three-dimensional space: frames of reference, vectors, and coordinate systems. , 1992, Annual review of neuroscience.

[49]  D. V. van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. , 2005, NeuroImage.

[50]  Clayton E. Curtis,et al.  Maintenance of Spatial and Motor Codes during Oculomotor Delayed Response Tasks , 2004, The Journal of Neuroscience.

[51]  B. Treutwein Adaptive psychophysical procedures , 1995, Vision Research.