Synaptic basis of persistent activity in prefrontal cortex in vivo and in organotypic cultures.

Persistent activity is observed in many cortical and subcortical brain regions, and may subserve a variety of functions. Within the prefrontal cortex (PFC), neurons transiently maintain information in working memory via persistent activity patterns; however, the mechanisms involved are largely unknown. The present study used intracellular recordings from deep layer PFC neurons in vivo and patch-clamp recordings from PFC neurons in organotypic brain slice cultures to examine the ionic mechanisms underlying persistent activity states evoked by various inputs. Persistent activity had consistent features regardless of the initiating stimulus; it was driven by non-NMDA glutamate receptors yet consisted of an initial GABA mediated component, followed by a prolonged synaptically mediated inward current that maintained the sustained depolarization on which rode many asynchronous GABA-mediated events. The stereotyped nature of the multiple-component persistent activity pattern reported here might be a common feature of interconnected cortical networks but within PFC could be related to the persistent activity required for working memory.

[1]  T. Honoré,et al.  Phencyclidine analogues inhibit NMDA-stimulated [3H]GABA release from cultured cortex neurons. , 1987, European journal of pharmacology.

[2]  J. Bockaert,et al.  NMDA- and kainate-evoked GABA release from striatal neurones differentiated in primary culture: Differential blocking by phencyclidine , 1988, Neuroscience Letters.

[3]  T. Sawaguchi,et al.  Catecholaminergic effects on neuronal activity related to a delayed response task in monkey prefrontal cortex. , 1990, Journal of neurophysiology.

[4]  K. Toyama,et al.  Laminar specificity of extrinsic cortical connections studied in coculture preparations , 1992, Neuron.

[5]  M. Steriade,et al.  A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  M Steriade,et al.  Cholinergic and noradrenergic modulation of the slow (approximately 0.3 Hz) oscillation in neocortical cells. , 1993, Journal of neurophysiology.

[7]  J. Bolz Cortical circuitry in a dish , 1994, Current Opinion in Neurobiology.

[8]  B. Moghaddam Recent basic findings in support of excitatory amino acid hypotheses of schizophrenia , 1994, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[9]  N. Spruston,et al.  Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons. , 1995, The Journal of physiology.

[10]  D. Contreras,et al.  Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  A. Grace,et al.  Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  T. Sejnowski,et al.  Reliability of spike timing in neocortical neurons. , 1995, Science.

[13]  Charles J. Wilson,et al.  The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  D. Plenz,et al.  Generation of high-frequency oscillations in local circuits of rat somatosensory cortex cultures. , 1996, Journal of neurophysiology.

[15]  D Contreras,et al.  Mechanisms of long‐lasting hyperpolarizations underlying slow sleep oscillations in cat corticothalamic networks. , 1996, The Journal of physiology.

[16]  P. Goldman-Rakic Regional and cellular fractionation of working memory. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[17]  D. Plenz,et al.  Neural dynamics in cortex-striatum co-cultures—II. Spatiotemporal characteristics of neuronal activity , 1996, Neuroscience.

[18]  M. Egan,et al.  Neurobiology of schizophrenia , 1997, Current Opinion in Neurobiology.

[19]  W. Schultz Dopamine neurons and their role in reward mechanisms , 1997, Current Opinion in Neurobiology.

[20]  Bita Moghaddam,et al.  Activation of Glutamatergic Neurotransmission by Ketamine: A Novel Step in the Pathway from NMDA Receptor Blockade to Dopaminergic and Cognitive Disruptions Associated with the Prefrontal Cortex , 1997, The Journal of Neuroscience.

[21]  S. Cragg,et al.  Dopamine is released spontaneously from developing midbrain neurons in organotypic culture , 1998, Neuroscience.

[22]  Joaquin M. Fuster,et al.  Distributed Memory for Both Short and Long Term , 1998, Neurobiology of Learning and Memory.

[23]  J. Seamans,et al.  D1 Receptor Modulation of Hippocampal–Prefrontal Cortical Circuits Integrating Spatial Memory with Executive Functions in the Rat , 1998, The Journal of Neuroscience.

[24]  W. Härtig,et al.  Selective in vivo fluorescence labelling of cholinergic neurons containing p75NTR in the rat basal forebrain , 1998, Brain Research.

[25]  Charles J. Wilson,et al.  Membrane potential synchrony of simultaneously recorded striatal spiny neurons in vivo , 1998, Nature.

[26]  A. Grace,et al.  Phencyclidine interferes with the hippocampal gating of nucleus accumbens neuronal activity in vivo , 1998, Neuroscience.

[27]  Takeshi Kawahara,et al.  Involvement of γ-aminobutyric acid neurotransmission in phencyclidine-induced dopamine release in the medial prefrontal cortex , 1998 .

[28]  P. Wahle,et al.  Patterns of spontaneous activity and morphology of interneuron types in organotypic cortex and thalamus–cortex cultures , 1999, Neuroscience.

[29]  T. Hökfelt,et al.  Neurocircuitries of the basal ganglia studied in organotypic cultures: focus on tyrosine hydroxylase, nitric oxide synthase and neuropeptide immunocytochemistry , 1999, Neuroscience.

[30]  X. Wang,et al.  Synaptic Basis of Cortical Persistent Activity: the Importance of NMDA Receptors to Working Memory , 1999, The Journal of Neuroscience.

[31]  A. Destexhe,et al.  Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. , 1999, Journal of neurophysiology.

[32]  Colin Blakemore,et al.  Development of Signals Influencing the Growth and Termination of Thalamocortical Axons in Organotypic Culture , 1999, Experimental Neurology.

[33]  J. Pierri,et al.  Altered GABA neurotransmission and prefrontal cortical dysfunction in schizophrenia , 1999, Biological Psychiatry.

[34]  B. Connors,et al.  Intrinsic firing patterns and whisker-evoked synaptic responses of neurons in the rat barrel cortex. , 1999, Journal of neurophysiology.

[35]  P. Goldman-Rakic,et al.  The physiological approach: functional architecture of working memory and disordered cognition in schizophrenia , 1999, Biological Psychiatry.

[36]  A. Destexhe,et al.  Synaptic background activity enhances the responsiveness of neocortical pyramidal neurons. , 2000, Journal of neurophysiology.

[37]  T. Sejnowski,et al.  Origin of slow cortical oscillations in deafferented cortical slabs. , 2000, Cerebral cortex.

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

[39]  Maria V. Sanchez-Vives,et al.  Cellular and network mechanisms of rhythmic recurrent activity in neocortex , 2000, Nature Neuroscience.

[40]  B. Lewis,et al.  Ventral tegmental area afferents to the prefrontal cortex maintain membrane potential 'up' states in pyramidal neurons via D(1) dopamine receptors. , 2000, Cerebral cortex.

[41]  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.

[42]  M Steriade,et al.  Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[43]  M. Steriade Impact of network activities on neuronal properties in corticothalamic systems. , 2001, Journal of neurophysiology.

[44]  Thoralf Opitz,et al.  Spontaneous development of synchronous oscillatory activity during maturation of cortical networks in vitro. , 2002, Journal of neurophysiology.

[45]  Anthony A Grace,et al.  Opposite Influences of Endogenous Dopamine D1 and D2 Receptor Activation on Activity States and Electrophysiological Properties of Striatal Neurons: Studies CombiningIn Vivo Intracellular Recordings and Reverse Microdialysis , 2002, The Journal of Neuroscience.

[46]  D. Plenz,et al.  Dendritic Calcium Encodes Striatal Neuron Output during Up-States , 2002, The Journal of Neuroscience.

[47]  J. D. Bruin,et al.  Cholinergic receptor blockade in prefrontal cortex and lesions of the nucleus basalis: implications for allocentric and egocentric spatial memory in rats , 2002, Behavioural Brain Research.

[48]  F. Edwards,et al.  Development of Rat CA1 Neurones in Acute Versus Organotypic Slices: Role of Experience in Synaptic Morphology and Activity , 2003, The Journal of physiology.