The roles of somatostatin-expressing (GIN) and fast-spiking inhibitory interneurons in UP-DOWN states of mouse neocortex.

The neocortex contains multiple types of inhibitory neurons whose properties suggest they may play different roles within the cortical circuit. By recording from three cell types during two distinct network states (UP and DOWN states) in vitro, we were able to quantify differences in firing characteristics between these cells during different network regimes. We recorded from regular-spiking (RS) excitatory cells and two types of inhibitory neurons, the fast-spiking (FS) neurons and GFP- (and somatostatin-) expressing inhibitory neurons (GIN), in layer 2/3 of slices from mouse somatosensory neocortex. Comparisons of firing characteristics between these cells during UP- and DOWN-states showed several patterns. First, of these cell types, only GIN cells fired persistently during DOWN-states, whereas all three cell types fired readily during UP-states. Second, the onset of firing and distribution of action potentials throughout UP-states differed by cell type, showing that FS cell UP-state firing occurred preferentially near the beginning of the UP-state, whereas the firing of RS cells was slower to develop at the start of the UP-state, and GIN cell firing was sustained throughout the duration of the UP-state. Finally, membrane potential and spike correlations between heterogeneous cell types were more pronounced during UP-states and, in the case of RS synapses onto GIN cells, varied throughout the UP-state. These results suggest that there is a division of labor between FS and GIN cells as the UP-state progresses and suggest that GIN cells could be important in the termination of UP-states.

[1]  Y. Kawaguchi,et al.  Two distinct activity patterns of fast-spiking interneurons during neocortical UP states , 2008, Proceedings of the National Academy of Sciences.

[2]  Karen L. Smith,et al.  Novel Hippocampal Interneuronal Subtypes Identified Using Transgenic Mice That Express Green Fluorescent Protein in GABAergic Interneurons , 2000, The Journal of Neuroscience.

[3]  P. Somogyi,et al.  Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex. , 1997, The Journal of physiology.

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

[5]  Michael A Long,et al.  Abrupt Maturation of a Spike-Synchronizing Mechanism in Neocortex , 2005, The Journal of Neuroscience.

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

[7]  A. Grinvald,et al.  Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[8]  D. McCormick,et al.  Post‐natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. , 1987, The Journal of physiology.

[9]  B. Connors,et al.  Thalamocortical responses of mouse somatosensory (barrel) cortexin vitro , 1991, Neuroscience.

[10]  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.

[11]  J. Hyvärinen,et al.  Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. , 1969, Journal of neurophysiology.

[12]  H. Markram,et al.  Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat , 2004, The Journal of physiology.

[13]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

[14]  D. Simons,et al.  Thalamocortical response transformation in the rat vibrissa/barrel system. , 1989, Journal of neurophysiology.

[15]  Arto V. Nurmikko,et al.  Pathway-Specific Feedforward Circuits between Thalamus and Neocortex Revealed by Selective Optical Stimulation of Axons , 2010, Neuron.

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

[17]  Maria V. Sanchez-Vives,et al.  Temperature modulation of slow and fast cortical rhythms. , 2010, Journal of neurophysiology.

[18]  D. Simons Response properties of vibrissa units in rat SI somatosensory neocortex. , 1978, Journal of neurophysiology.

[19]  D. Prince,et al.  Temperature dependence of intrinsic membrane properties and synaptic potentials in hippocampal CA1 neurons in vitro , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  B. Connors,et al.  Two networks of electrically coupled inhibitory neurons in neocortex , 1999, Nature.

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

[22]  A. Destexhe,et al.  The high-conductance state of neocortical neurons in vivo , 2003, Nature Reviews Neuroscience.

[23]  B. Bean The action potential in mammalian central neurons , 2007, Nature Reviews Neuroscience.

[24]  P. Somogyi,et al.  Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo , 2003, Nature.

[25]  Michael Rudolph,et al.  The high-conductance state of neocortical neurons in vivo , 2003, Nature Reviews Neuroscience.

[26]  D. McCormick,et al.  Turning on and off recurrent balanced cortical activity , 2003, Nature.

[27]  John R Huguenard,et al.  Electrophysiological classification of somatostatin-positive interneurons in mouse sensorimotor cortex. , 2006, Journal of neurophysiology.

[28]  Erika E Fanselow,et al.  Selective, state-dependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex. , 2008, Journal of neurophysiology.

[29]  D. McCormick,et al.  Neocortical Network Activity In Vivo Is Generated through a Dynamic Balance of Excitation and Inhibition , 2006, The Journal of Neuroscience.

[30]  A. Bacci,et al.  Enhancement of Spike-Timing Precision by Autaptic Transmission in Neocortical Inhibitory Interneurons , 2006, Neuron.

[31]  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.

[32]  Maria V. Sanchez-Vives,et al.  Cellular and network mechanisms of slow oscillatory activity (<1 Hz) and wave propagations in a cortical network model. , 2003, Journal of neurophysiology.

[33]  C. Petersen,et al.  Membrane Potential Dynamics of GABAergic Neurons in the Barrel Cortex of Behaving Mice , 2010, Neuron.

[34]  J. Deuchars,et al.  Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. , 1996, The Journal of physiology.

[35]  Michael Rudolph,et al.  Characterization of synaptic conductances and integrative properties during electrically induced EEG-activated states in neocortical neurons in vivo. , 2005, Journal of neurophysiology.

[36]  M. Steriade,et al.  Natural waking and sleep states: a view from inside neocortical neurons. , 2001, Journal of neurophysiology.

[37]  Emery N Brown,et al.  Activity in the barrel cortex during active behavior and sleep. , 2010, Journal of neurophysiology.

[38]  B. Connors,et al.  Two dynamically distinct inhibitory networks in layer 4 of the neocortex. , 2003, Journal of neurophysiology.

[39]  T R Vidyasagar,et al.  Membrane properties and spike generation in rat visual cortical cells during reversible cooling , 2000, The Journal of physiology.

[40]  S. Cruikshank,et al.  Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex , 2007, Nature Neuroscience.

[41]  William R. Softky,et al.  Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. , 1996, Journal of neurophysiology.