Left frontal eye field remembers “where” but not “what”

Short-term memory of basic stimulus features seems to rely upon low-level functional components of the visual pathways. By using a repetition priming paradigm, we previously showed that visual area V5/MT is important for holding motion direction information, but not spatial position information. Here we extend our previous findings and investigate the possible locus of spatial position priming. We compare the effect of repetitive transcranial magnetic stimulation (rTMS) over right angular gyrus and left and right frontal eye fields on priming for spatial position and motion direction. TMS over left frontal eye field selectively and significantly reduced priming for spatial position but there was no significant effect of TMS over right parietal or right frontal eye field. These results suggest that FEF neurons are implicated in short-term memory storage of spatial position, and extend and support the idea that memory for basic stimulus features is retained within the sensory areas that respond to primary stimulus attributes. They add to a growing body of evidence that the frontal eye fields are involved in many visual functions independent of eye movements.

[1]  Paul V McGraw,et al.  Motion-Sensitive Neurones in V5/MT Modulate Perceived Spatial Position , 2004, Current Biology.

[2]  I. Biederman,et al.  Localizing the cortical region mediating visual awareness of object identity. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Walsh,et al.  Transcranial magnetic stimulation: a neurochromometrics of mind. , 2003 .

[4]  Gianluca Campana,et al.  Priming of motion direction and area V5/MT: a test of perceptual memory. , 2002, Cerebral cortex.

[5]  S Magnussen,et al.  The psychophysics of perceptual memory , 1999, Psychological research.

[6]  B. Gaymard,et al.  The frontal eye field is involved in spatial short-term memory but not in reflexive saccade inhibition , 1999, Experimental Brain Research.

[7]  M. Rushworth,et al.  A primer of magnetic stimulation as a tool for neuropsychology. , 1999, Neuropsychologia.

[8]  Chris Rorden,et al.  Transcranial magnetic stimulation of the left human frontal eye fields eliminates the cost of invalid endogenous cues , 2005, Neuropsychologia.

[9]  Neil G. Muggleton,et al.  Timing of Target Discrimination in Human Frontal Eye Fields , 2004, Journal of Cognitive Neuroscience.

[10]  R. Rafal,et al.  Effects of Parietal Lesions in Humans on Color and Location Priming , 1998, Journal of Cognitive Neuroscience.

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

[12]  N. P. Bichot,et al.  Priming in Macaque Frontal Cortex during Popout Visual Search: Feature-Based Facilitation and Location-Based Inhibition of Return , 2002, The Journal of Neuroscience.

[13]  A. Cowey,et al.  Normal discrimination performance accompanied by priming deficits in monkeys with V4 or TEO lesions. , 2000, Neuroreport.

[14]  Chi-Hung Juan,et al.  Human frontal eye fields and visual search. , 2003, Journal of neurophysiology.

[15]  Alan Cowey,et al.  Temporal aspects of visual search studied by transcranial magnetic stimulation , 1997, Neuropsychologia.

[16]  Veit Stuphorn,et al.  Chronometry of visual responses in frontal eye field, supplementary eye field, and anterior cingulate cortex. , 2005, Journal of neurophysiology.

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

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

[19]  Neil G. Muggleton,et al.  On the roles of the human frontal eye fields and parietal cortex in visual search , 2006 .

[20]  M. Mesulam,et al.  Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[21]  A. Berthoz,et al.  The neural basis of egocentric and allocentric coding of space in humans: a functional magnetic resonance study , 2000, Experimental Brain Research.

[22]  Sylvie Chokron,et al.  Orienting of attention in left unilateral neglect , 2002, Neuroscience & Biobehavioral Reviews.

[23]  S. Magnussen Low-level memory processes in vision , 2000, Trends in Neurosciences.

[24]  Alvaro Pascual-Leone,et al.  Repetitive transcranial magnetic stimulation of human area MT/V5 disrupts perception and storage of the motion aftereffect , 2002, Neuropsychologia.

[25]  Kenneth F. Valyear,et al.  Human parietal cortex in action , 2006, Current Opinion in Neurobiology.

[26]  T. Pasternak,et al.  Working memory in primate sensory systems , 2005, Nature Reviews Neuroscience.

[27]  T. Pasternak,et al.  The multiple roles of visual cortical areas MT/MST in remembering the direction of visual motion. , 2000, Cerebral cortex.

[28]  J. Mattingley,et al.  Fast and slow parietal pathways mediate spatial attention , 2004, Nature Neuroscience.

[29]  S. Magnussen,et al.  Fast perceptual priming in the left and right hemispheres. , 2006, Scandinavian journal of psychology.

[30]  Takashi R Sato,et al.  Search Efficiency but Not Response Interference Affects Visual Selection in Frontal Eye Field , 2001, Neuron.

[31]  Jeffrey D. Schall,et al.  Effect of target-distractor similarity on FEF visual selection in the absence of the target , 2003, Experimental Brain Research.

[32]  K. Nakayama,et al.  Priming of popout: III. A short-term implicit memory system beneficial for rapid target selection , 2000 .

[33]  Scott T. Grafton,et al.  Reductions in neural activity underlie behavioral components of repetition priming , 2005, Nature Neuroscience.

[34]  M. Rushworth,et al.  Complementary localization and lateralization of orienting and motor attention , 2001, Nature Neuroscience.

[35]  Frank Rösler,et al.  Topography of brain electrical activity dissociates the retrieval of spatial versus verbal information from episodic long-term memory in humans , 1997, Neuroscience Letters.

[36]  Jeffrey D Schall,et al.  On the role of frontal eye field in guiding attention and saccades , 2004, Vision Research.

[37]  S. Pollmann,et al.  Covert Reorienting and Inhibition of Return: An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[38]  R. Henson Neuroimaging studies of priming , 2003, Progress in Neurobiology.

[39]  K. Nakayama,et al.  Priming of pop-out: II. The role of position , 1996, Perception & psychophysics.

[40]  J. Bullier Integrated model of visual processing , 2001, Brain Research Reviews.

[41]  E Tulving,et al.  Priming and human memory systems. , 1990, Science.

[42]  K. Nakayama,et al.  Priming of pop-out: I. Role of features , 1994, Memory & cognition.

[43]  Gianluca Campana,et al.  Visual area V5/MT remembers "what" but not "where". , 2004, Cerebral cortex.