Diversity of Gain Modulation by Noise in Neocortical Neurons: Regulation by the Slow Afterhyperpolarization Conductance

Neuronal firing is known to depend on the variance of synaptic input as well as the mean input current. Several studies suggest that input variance, or “noise,” has a divisive effect, reducing the slope or gain of the firing frequency–current (f–I) relationship. We measured the effects of current noise on f–I relationships in pyramidal neurons and fast-spiking (FS) interneurons in slices of rat sensorimotor cortex. In most pyramidal neurons, noise had a multiplicative effect on the steady-state f–I relationship, increasing gain. In contrast, noise reduced gain in FS interneurons. Gain enhancement in pyramidal neurons increased with stimulus duration and was correlated with the amplitude of the slow afterhyperpolarization (sAHP), a major mechanism of spike-frequency adaptation. The 5-HT2 receptor agonist α-methyl-5-HT reduced the sAHP and eliminated gain increases, whereas augmenting the sAHP conductance by spike-triggered dynamic-current clamp enhanced the gain increase. These results indicate that the effects of noise differ fundamentally between classes of neocortical neurons, depending on specific biophysical properties including the sAHP conductance. Thus, noise from background synaptic input may enhance network excitability by increasing gain in pyramidal neurons with large sAHPs and reducing gain in inhibitory FS interneurons.

[1]  A. Keller,et al.  Intrinsic circuitry and physiological properties of pyramidal neurons in rat barrel cortex , 1997, Experimental Brain Research.

[2]  R. Nicoll,et al.  Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. , 1984, The Journal of physiology.

[3]  R K Powers,et al.  Effects of background noise on the response of rat and cat motoneurones to excitatory current transients. , 1996, The Journal of physiology.

[4]  L. Palmer,et al.  Response to Contrast of Electrophysiologically Defined Cell Classes in Primary Visual Cortex , 2003, The Journal of Neuroscience.

[5]  Michael Rudolph,et al.  Do Neocortical Pyramidal Neurons Display Stochastic Resonance? , 2001, Journal of Computational Neuroscience.

[6]  Walter Senn,et al.  Minimal Models of Adapted Neuronal Response to In VivoLike Input Currents , 2004, Neural Computation.

[7]  B. Sakmann,et al.  Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons , 1997, The Journal of physiology.

[8]  P. Schwindt,et al.  Long-lasting reduction of excitability by a sodium-dependent potassium current in cat neocortical neurons. , 1989, Journal of neurophysiology.

[9]  L A JEFFRESS,et al.  A place theory of sound localization. , 1948, Journal of comparative and physiological psychology.

[10]  Emilio Salinas,et al.  Gain Modulation A Major Computational Principle of the Central Nervous System , 2000, Neuron.

[11]  A. Erisir,et al.  Function of specific K(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons. , 1999, Journal of neurophysiology.

[12]  R. Foehring,et al.  The ontogeny of repetitive firing and its modulation by norepinephrine in rat neocortical neurons. , 1993, Brain research. Developmental brain research.

[13]  O. Bertrand,et al.  Oscillatory Synchrony between Human Extrastriate Areas during Visual Short-Term Memory Maintenance , 2001, The Journal of Neuroscience.

[14]  A. Reyes Synchrony-dependent propagation of firing rate in iteratively constructed networks in vitro , 2003, Nature Neuroscience.

[15]  L. Symon,et al.  Changes in Extracellular Calcium Activity in Cerebral Ischaemia , 1981, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[16]  Carrie J. McAdams,et al.  Effects of Attention on Orientation-Tuning Functions of Single Neurons in Macaque Cortical Area V4 , 1999, The Journal of Neuroscience.

[17]  Christof Koch,et al.  Shunting Inhibition Does Not Have a Divisive Effect on Firing Rates , 1997, Neural Computation.

[18]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. I. Establishment of cell classes , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  P König,et al.  Direct physiological evidence for scene segmentation by temporal coding. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[20]  W. Spain Serotonin has different effects on two classes of Betz cells from the cat. , 1994, Journal of neurophysiology.

[21]  M. Massimini,et al.  Extracellular calcium fluctuations and intracellular potentials in the cortex during the slow sleep oscillation. , 2001, Journal of neurophysiology.

[22]  Brent Doiron,et al.  Deterministic Multiplicative Gain Control with Active Dendrites , 2005, The Journal of Neuroscience.

[23]  G. Kinney,et al.  Dynamic Influences on Coincidence Detection in Neocortical Pyramidal Neurons , 2004, The Journal of Neuroscience.

[24]  Andreas V. M. Herz,et al.  A Universal Model for Spike-Frequency Adaptation , 2003, Neural Computation.

[25]  A. Reyes,et al.  In vitro analysis of optimal stimuli for phase-locking and time-delayed modulation of firing in avian nucleus laminaris neurons , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[27]  P. Schwindt,et al.  Quantitative analysis of firing properties of pyramidal neurons from layer 5 of rat sensorimotor cortex. , 1997, Journal of neurophysiology.

[28]  R. Metherate,et al.  Modulation of cellular excitability in neocortex: Muscarinic receptor and second messenger‐mediated actions of acetylcholine , 1994, Synapse.

[29]  D. Asdourian,et al.  Effects of thalamic and limbic system lesions on self-stimulation. , 1966, Journal of comparative and physiological psychology.

[30]  Wulfram Gerstner,et al.  SPIKING NEURON MODELS Single Neurons , Populations , Plasticity , 2002 .

[31]  A. Friedman,et al.  Stepwise repolarization from Ca2+ plateaus in neocortical pyramidal cells: evidence for nonhomogeneous distribution of HVA Ca2+ channels in dendrites , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  H. Robinson,et al.  Threshold firing frequency-current relationships of neurons in rat somatosensory cortex: type 1 and type 2 dynamics. , 2004, Journal of neurophysiology.

[33]  A. A. Velumian,et al.  Whole-cell recording of the Ca2+-dependent slow afterhyperpolarization in hippocampal neurones: effects of internally applied anions , 1994, Pflügers Archiv.

[34]  E. Niebur,et al.  Growth patterns in the developing brain detected by using continuum mechanical tensor maps , 2022 .

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

[36]  W. Senn,et al.  Neocortical pyramidal cells respond as integrate-and-fire neurons to in vivo-like input currents. , 2003, Journal of neurophysiology.

[37]  Andrea Hasenstaub,et al.  Barrages of Synaptic Activity Control the Gain and Sensitivity of Cortical Neurons , 2003, The Journal of Neuroscience.

[38]  M. Madeja,et al.  Do neurons have a reserve of sodium channels for the generation of action potentials? A study on acutely isolated CA1 neurons from the guinea‐pig hippocampus , 2000, The European journal of neuroscience.

[39]  G. P. Moore,et al.  SENSITIVITY OF NEURONES IN APLYSIA TO TEMPORAL PATTERN OF ARRIVING IMPULSES. , 1963, The Journal of experimental biology.

[40]  G. Stuart,et al.  Backpropagation of Physiological Spike Trains in Neocortical Pyramidal Neurons: Implications for Temporal Coding in Dendrites , 2000, The Journal of Neuroscience.

[41]  T. Sejnowski,et al.  Effects of cholinergic modulation on responses of neocortical neurons to fluctuating input. , 1997, Cerebral cortex.

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

[43]  Stefan Treue,et al.  Feature-based attention influences motion processing gain in macaque visual cortex , 1999, Nature.

[44]  Frances S. Chance,et al.  Gain Modulation from Background Synaptic Input , 2002, Neuron.

[45]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  R. Andrade,et al.  Serotonergic regulation of calcium‐activated potassium currents in rodent prefrontal cortex , 2005, The European journal of neuroscience.

[47]  B. Sakmann,et al.  Action potential initiation and propagation in rat neocortical pyramidal neurons , 1997, The Journal of physiology.

[48]  H. Ohmori,et al.  Tonotopic Specialization of Auditory Coincidence Detection in Nucleus Laminaris of the Chick , 2005, The Journal of Neuroscience.

[49]  Kenneth O. Johnson,et al.  Synchrony: a neuronal mechanism for attentional selection? , 2002, Current Opinion in Neurobiology.

[50]  M. Gutnick,et al.  Slow inactivation of Na+ current and slow cumulative spike adaptation in mouse and guinea‐pig neocortical neurones in slices. , 1996, The Journal of physiology.

[51]  Adrienne L Fairhall,et al.  Two-Dimensional Time Coding in the Auditory Brainstem , 2005, The Journal of Neuroscience.

[52]  Dany Arsenault,et al.  Gain modulation by serotonin in pyramidal neurones of the rat prefrontal cortex , 2005, The Journal of physiology.

[53]  P. Schwindt,et al.  Mechanisms underlying burst and regular spiking evoked by dendritic depolarization in layer 5 cortical pyramidal neurons. , 1999, Journal of neurophysiology.

[54]  P. Schwindt,et al.  Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes. , 1988, Journal of neurophysiology.

[55]  R. Silver,et al.  Shunting Inhibition Modulates Neuronal Gain during Synaptic Excitation , 2003, Neuron.

[56]  Jorge V. José,et al.  Synchronization as a mechanism for attentional gain modulation , 2004, Neurocomputing.

[57]  Jorge V. José,et al.  Inhibitory synchrony as a mechanism for attentional gain modulation , 2004, Journal of Physiology-Paris.

[58]  B. Connors,et al.  Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[59]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[60]  B. Sakmann,et al.  Dendritic mechanisms underlying the coupling of the dendritic with the axonal action potential initiation zone of adult rat layer 5 pyramidal neurons , 2001, The Journal of physiology.

[61]  C. Radici,et al.  Postnatal differentiation of firing properties and morphological characteristics in layer V pyramidal neurons of the sensorimotor cortex , 1998, Neuroscience.

[62]  M. Konishi,et al.  A circuit for detection of interaural time differences in the brain stem of the barn owl , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[64]  C. Gray,et al.  Physiological properties of inhibitory interneurons in cat striate cortex. , 1997, Cerebral cortex.

[65]  P. Schwindt,et al.  Norepinephrine selectively reduces slow Ca2+- and Na+-mediated K+ currents in cat neocortical neurons. , 1989, Journal of neurophysiology.

[66]  T. Sejnowski,et al.  Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity , 2003, Neuroscience.

[67]  W. Senn,et al.  Top-down dendritic input increases the gain of layer 5 pyramidal neurons. , 2004, Cerebral cortex.

[68]  Walther Akemann,et al.  Transgenic mice expressing a fluorescent in vivo label in a distinct subpopulation of neocortical layer 5 pyramidal cells , 2004, The Journal of comparative neurology.