Comparison of Neural Activity Related to Working Memory in Primate Dorsolateral Prefrontal and Posterior Parietal Cortex

Neurons in a distributed network of cortical and subcortical areas continue to discharge after the presentation and disappearance of stimuli, providing a neural correlate for working memory. While it is thought that the prefrontal cortex plays a central role in this network, the relative contributions of other brain areas are not as well understood. In order to compare the contributions of the dorsolateral prefrontal and posterior parietal cortex, we recorded neurophysiological activity in monkeys trained to perform two different visuo-spatial working memory tasks: a Match/Nonmatch task, and a Spatial Delayed-Match-to-Sample Task. Neurons in both areas exhibited discharges in the delay periods of the tasks that could be classified in two forms. Sustained discharges persisted after the presentation of a stimulus in the receptive field with a constant or declining rate. Anticipatory responses increased in rate during the delay period, often appearing after presentation of a stimulus out of the receptive field. Despite similarities, we uncovered distinct differences between patterns of delay period in each brain area. Only in the prefrontal cortex sustained responses related to the original stimulus survived presentation of a second stimulus, in the context of the Match/Nonmatch task. Our results provide insights on the nature of processing in two areas active during working memory, and on the unique role of the prefrontal cortex in memory maintenance.

[1]  R. Desimone,et al.  Activity of neurons in anterior inferior temporal cortex during a short- term memory task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[3]  P. Goldman-Rakic,et al.  Division of labor among distinct subtypes of inhibitory neurons in a cortical microcircuit of working memory. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[4]  J. Fuster,et al.  Mnemonic and predictive functions of cortical neurons in a memory task , 1992, Neuroreport.

[5]  Zheng Liu,et al.  Short-Term Memory Trace in Rapidly Adapting Synapses of Inferior Temporal Cortex , 2008, PLoS Comput. Biol..

[6]  Natasha Sigala Visual Working Memory and Delay Activity in Highly Selective Neurons in the Inferior Temporal Cortex , 2009, Front. Syst. Neurosci..

[7]  S. Wise,et al.  Visuospatial versus visuomotor activity in the premotor and prefrontal cortex of a primate , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  David L. Sheinberg,et al.  Neural Dynamics in Inferior Temporal Cortex during a Visual Working Memory Task , 2009, The Journal of Neuroscience.

[9]  R. Desimone,et al.  Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque , 1996, The Journal of Neuroscience.

[10]  G. Elston Pyramidal Cells of the Frontal Lobe: All the More Spinous to Think With , 2000, The Journal of Neuroscience.

[11]  E. Procyk,et al.  The primate working memory networks , 2004, Cognitive, affective & behavioral neuroscience.

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

[13]  Christian K. Machens,et al.  Behavioral / Systems / Cognitive Functional , But Not Anatomical , Separation of “ What ” and “ When ” in Prefrontal Cortex , 2009 .

[14]  T. Sejnowski,et al.  Dopamine D1/D5 receptor modulation of excitatory synaptic inputs to layer V prefrontal cortex neurons. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Huaixing Wang,et al.  A specialized NMDA receptor function in layer 5 recurrent microcircuitry of the adult rat prefrontal cortex , 2008, Proceedings of the National Academy of Sciences.

[16]  C. Constantinidis,et al.  Persistent discharges in the prefrontal cortex of monkeys naive to working memory tasks. , 2007, Cerebral cortex.

[17]  M. Tsodyks,et al.  Synaptic Theory of Working Memory , 2008, Science.

[18]  R. Romo,et al.  Neuronal correlates of parametric working memory in the prefrontal cortex , 1999, Nature.

[19]  R. Romo,et al.  Timing and neural encoding of somatosensory parametric working memory in macaque prefrontal cortex. , 2003, Cerebral cortex.

[20]  T. Sejnowski,et al.  Dopamine-mediated stabilization of delay-period activity in a network model of prefrontal cortex. , 2000, Journal of neurophysiology.

[21]  Albert Compte,et al.  Temporal properties of posterior parietal neuron discharges during working memory and passive viewing. , 2007, Journal of neurophysiology.

[22]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[23]  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.

[24]  R. Romo,et al.  Neuronal correlates of decision-making in secondary somatosensory cortex , 2002, Nature Neuroscience.

[25]  M. A. Steinmetz,et al.  Neuronal activity in posterior parietal area 7a during the delay periods of a spatial memory task. , 1996, Journal of neurophysiology.

[26]  Christos Constantinidis,et al.  A software solution for the control of visual behavioral experimentation , 2005, Journal of Neuroscience Methods.

[27]  J. Csicsvari,et al.  Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. , 2000, Journal of neurophysiology.

[28]  CR Yang,et al.  Dopamine D1 receptor actions in layers V-VI rat prefrontal cortex neurons in vitro: modulation of dendritic-somatic signal integration , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[30]  Christos Constantinidis,et al.  Effects of task and coordinate frame of attention in area 7a of the primate posterior parietal cortex. , 2011, Journal of vision.

[31]  Zhen Yan,et al.  Potentiation of NMDA receptor currents by dopamine D1 receptors in prefrontal cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[33]  Yasushi Miyashita,et al.  Active Maintenance of Associative Mnemonic Signal in Monkey Inferior Temporal Cortex , 2005, Neuron.

[34]  G. Elston The pyramidal neuron in occipital, temporal and prefrontal cortex of the owl monkey (Aotus trivirgatus): regional specialization in cell structure , 2003, The European journal of neuroscience.

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

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

[37]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections , 1989, The Journal of comparative neurology.

[38]  M. D’Esposito Working memory. , 2008, Handbook of clinical neurology.

[39]  Xiao-Jing Wang Synaptic reverberation underlying mnemonic persistent activity , 2001, Trends in Neurosciences.

[40]  E. Miller,et al.  Timecourse of object‐related neural activity in the primate prefrontal cortex during a short‐term memory task , 2002, The European journal of neuroscience.