Heterogeneity in the pyramidal network of the medial prefrontal cortex

The prefrontal cortex is specially adapted to generate persistent activity that outlasts stimuli and is resistant to distractors, presumed to be the basis of working memory. The pyramidal network that supports this activity is unknown. Multineuron patch-clamp recordings in the ferret medial prefrontal cortex showed a heterogeneity of synapses interconnecting distinct subnetworks of different pyramidal cells. One subnetwork was similar to the pyramidal network commonly found in primary sensory areas, consisting of accommodating pyramidal cells interconnected with depressing synapses. The other subnetwork contained complex pyramidal cells with dual apical dendrites displaying nonaccommodating discharge patterns; these cells were hyper-reciprocally connected with facilitating synapses displaying pronounced synaptic augmentation and post-tetanic potentiation. These cellular, synaptic and network properties could amplify recurrent interactions between pyramidal neurons and support persistent activity in the prefrontal cortex.

[1]  P S Goldman-Rakic,et al.  Mediodorsal nucleus: Areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkeys , 1988, The Journal of comparative neurology.

[2]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

[3]  K. Stratford,et al.  Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  J. Deuchars,et al.  Single axon excitatory postsynaptic potentials in neocortical interneurons exhibit pronounced paired pulse facilitation , 1993, Neuroscience.

[5]  J. Deuchars,et al.  Large, deep layer pyramid-pyramid single axon EPSPs in slices of rat motor cortex display paired pulse and frequency-dependent depression, mediated presynaptically and self-facilitation, mediated postsynaptically. , 1993, Journal of neurophysiology.

[6]  Rafael Yuste,et al.  Ca2+ accumulations in dendrites of neocortical pyramidal neurons: An apical band and evidence for two functional compartments , 1994, Neuron.

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

[8]  P. Goldman-Rakic.  Architecture of the Prefrontal Cortex and the Central Executive , 1995, Annals of the New York Academy of Sciences.

[9]  R. Douglas,et al.  The role of synapses in cortical computation , 1996, Journal of neurocytology.

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

[11]  L. Abbott,et al.  Synaptic Depression and Cortical Gain Control , 1997, Science.

[12]  H. Markram,et al.  The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[13]  H. Markram.  A network of tufted layer 5 pyramidal neurons. , 1997, Cerebral cortex.

[14]  Thomas J. Carew,et al.  Multiple overlapping processes underlying short-term synaptic enhancement , 1997, Trends in Neurosciences.

[15]  H. Markram,et al.  Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. , 1997, The Journal of physiology.

[16]  L. Abbott,et al.  A Quantitative Description of Short-Term Plasticity at Excitatory Synapses in Layer 2/3 of Rat Primary Visual Cortex , 1997, The Journal of Neuroscience.

[17]  A. Thomson.  Activity‐dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro , 1997, The Journal of physiology.

[18]  J. Magee.  Dendritic Hyperpolarization-Activated Currents Modify the Integrative Properties of Hippocampal CA1 Pyramidal Neurons , 1998, The Journal of Neuroscience.

[19]  S. Hestrin,et al.  Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex , 1998, Nature Neuroscience.

[20]  H. Markram,et al.  Differential signaling via the same axon of neocortical pyramidal neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[21]  P. Somogyi,et al.  Target-cell-specific facilitation and depression in neocortical circuits , 1998, Nature Neuroscience.

[22]  B. Sakmann,et al.  A new cellular mechanism for coupling inputs arriving at different cortical layers , 1999, Nature.

[23]  K. Martin,et al.  Intracortical excitation of spiny neurons in layer 4 of cat striate cortex in vitro. , 1999, Cerebral cortex.

[24]  B. Sakmann,et al.  Developmental Switch in the Short-Term Modification of Unitary EPSPs Evoked in Layer 2/3 and Layer 5 Pyramidal Neurons of Rat Neocortex , 1999, The Journal of Neuroscience.

[25]  B. Sakmann,et al.  Calcium electrogenesis in distal apical dendrites of layer 5 pyramidal cells at a critical frequency of back-propagating action potentials. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[26]  S. Nelson,et al.  Multiple forms of short-term plasticity at excitatory synapses in rat medial prefrontal cortex. , 2000, Journal of neurophysiology.

[27]  A. Thomson.  Facilitation, augmentation and potentiation at central synapses , 2000, Trends in Neurosciences.

[28]  H. Markram,et al.  Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. , 2000, Science.

[29]  T. Sejnowski,et al.  Neurocomputational models of working memory , 2000, Nature Neuroscience.

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

[31]  M. Larkum,et al.  High I(h) channel density in the distal apical dendrite of layer V pyramidal cells increases bidirectional attenuation of EPSPs. , 2001, Journal of neurophysiology.

[32]  P. Goldman-Rakic,et al.  Presynaptic regulation of recurrent excitation by D1 receptors in prefrontal circuits. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[33]  David A. McCormick,et al.  Brain calculus: neural integration and persistent activity , 2001, Nature Neuroscience.

[34]  Paul A. Rhodes,et al.  Apical tuft input efficacy in layer 5 pyramidal cells from rat visual cortex , 2001, The Journal of physiology.

[35]  Yun Wang,et al.  Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2-5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro. , 2002, Cerebral cortex.

[36]  W. Regehr,et al.  Short-term synaptic plasticity. , 2002, Annual review of physiology.

[37]  D. Amit,et al.  Retrospective and prospective persistent activity induced by Hebbian learning in a recurrent cortical network , 2003, The European journal of neuroscience.

[38]  G. Elston.  Cortex, cognition and the cell: new insights into the pyramidal neuron and prefrontal function. , 2003, Cerebral cortex.

[39]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

[40]  Paul Leonard Gabbott,et al.  Prefrontal cortex in the rat: Projections to subcortical autonomic, motor, and limbic centers , 2005, The Journal of comparative neurology.

[41]  Alex M Thomson,et al.  Excitatory connections made by presynaptic cortico-cortical pyramidal cells in layer 6 of the neocortex. , 2005, Cerebral cortex.

[42]  H. Markram,et al.  The neocortical microcircuit as a tabula rasa. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Alex M Thomson,et al.  Layer 6 cortico-thalamic pyramidal cells preferentially innervate interneurons and generate facilitating EPSPs. , 2006, Cerebral cortex.

[44]  R. K. Simpson.  Nature Neuroscience , 2022 .