Different Neuronal Computations of Spatial Working Memory for Multiple Locations within versus across Visual Hemifields

Spatial working memory is one of the most studied cognitive functions, serving as a model system to decipher computational principles of the brain. Although neuronal mechanisms for remembering a single location have been well elucidated, little is known about memory for multiple locations. Here, we examined the activities of prefrontal neurons during monkeys remembered positions of one or two visual cue(s). When the two cues were presented across the left and right visual fields, neurons exhibited a comparable response to the activity for the preferred cue presented alone. When the two cues were presented within the same hemifield, neurons exhibited an intermediate response between those to the individual cues. Subsequent computer simulations predicted a lower signal-to-noise ratio in the latter condition, which was further verified by behavioral experiments. Considering the separation of contralateral and ipsilateral visual processing, the lateral inhibition in local circuits might implicitly determine different neuronal computations and memory capacities for bilateral and unilateral displays.

[1]  Julio C. Martinez-Trujillo,et al.  Prefrontal Neurons of Opposite Spatial Preference Display Distinct Target Selection Dynamics , 2013, The Journal of Neuroscience.

[2]  E. Miller,et al.  Memory fields of neurons in the primate prefrontal cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Aysenil Belger,et al.  Interhemispheric Interaction: How Do the Hemispheres Divide and Conquer a Task? , 1990, Cortex.

[4]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. III. Memory-contingent visual and saccade responses. , 1983, Journal of neurophysiology.

[5]  Jesper Tegnér,et al.  Mechanism for top-down control of working memory capacity , 2009, Proceedings of the National Academy of Sciences.

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

[7]  G. E. Alexander,et al.  Neuron Activity Related to Short-Term Memory , 1971, Science.

[8]  Xiao-Jing Wang,et al.  The importance of mixed selectivity in complex cognitive tasks , 2013, Nature.

[9]  P. Goldman-Rakic,et al.  Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. , 2000, Cerebral cortex.

[10]  Masaki Tanaka,et al.  Smooth Pursuit Eye Movements , 2018 .

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

[12]  Stefan Treue,et al.  Multifocal Attention Filters Targets from Distracters within and beyond Primate MT Neurons' Receptive Field Boundaries , 2011, Neuron.

[13]  Alex S. Ferecskó,et al.  The fractions of short- and long-range connections in the visual cortex , 2009, Proceedings of the National Academy of Sciences.

[14]  Earl K Miller,et al.  The representation of multiple objects in prefrontal neuronal delay activity. , 2007, Cerebral cortex.

[15]  P. Goldman-Rakic.  Cellular basis of working memory , 1995, Neuron.

[16]  Xiao-Jing Wang,et al.  From Distributed Resources to Limited Slots in Multiple-Item Working Memory: A Spiking Network Model with Normalization , 2012, The Journal of Neuroscience.

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

[18]  Masaki Tanaka,et al.  Neuronal Correlates of Multiple Top–Down Signals during Covert Tracking of Moving Objects in Macaque Prefrontal Cortex , 2012, Journal of Cognitive Neuroscience.

[19]  R. Andersen,et al.  Memory related motor planning activity in posterior parietal cortex of macaque , 1988, Experimental Brain Research.

[20]  G. Turrigiano.  Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. , 2011, Annual review of neuroscience.

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

[22]  H. Hultsch.  Time window and unit capacity: dual constraints on the acquisition of serial information in songbirds , 1992, Journal of Comparative Physiology A.

[23]  Paul Leonard Gabbott,et al.  Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey: II. Quantitative areal and laminar distributions , 1996, The Journal of comparative neurology.

[24]  Marius Usher,et al.  Short Term Memory and Selection Processes in a Frontal-Lobe Model , 1999 .

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

[26]  P. Goldman-Rakic,et al.  Interdigitation of contralateral and ipsilateral columnar projections to frontal association cortex in primates. , 1982, Science.

[27]  John H. R. Maunsell,et al.  Attentional modulation of visual motion processing in cortical areas MT and MST , 1996, Nature.

[28]  H. Niki,et al.  Prefrontal cortical unit activity and delayed alternation performance in monkeys. , 1971, Journal of neurophysiology.

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

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

[31]  J. Sergent,et al.  Furtive incursions into bicameral minds. Integrative and coordinating role of subcortical structures. , 1990, Brain : a journal of neurology.

[32]  Jean-François Delvenne,et al.  The capacity of visual short-term memory within and between hemifields , 2005, Cognition.

[33]  P. Goldman-Rakic,et al.  Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. , 1999, Journal of neurophysiology.