Neuromodulation of Spike-Timing Precision in Sensory Neurons

111

163

The piriform (or primary olfactory) cortex is a trilaminar structure that is the first cortical destination of olfactory information, receiving monosynaptic input from the olfactory bulb. Here, we show that the main input layer of the piriform cortex, layer II, is dominated by two classes of principal neurons, superficial pyramidal (SP) and semilunar (SL) cells, with strikingly different properties. Action potentials in SP cells are followed by a Ni 2ϩ -sensitive afterdepolarization that promotes burst firing, whereas SL cells fire nonbursting action potentials that are followed by a powerful afterhyperpolarization. Synaptic inputs from the olfactory bulb onto SP cells exhibit prominent paired-pulse facilitation, which is attributable to residual presynaptic Ca 2ϩ and a low probability of neurotransmitter release. In contrast, the same inputs onto SL cells do not facilitate. These distinctive synaptic and firing properties cause SP and SL cells to respond differently to in vivo-like bursts of afferent stimulation: SP cells tend to fire bursts of output action potentials at a higher frequency than the input, whereas SL cells tend to fire at a lower frequency than the input. When connected together in the canonical circuit of the piriform cortex, SP and SL cells transform the pattern of synaptic inputs they receive from the olfactory bulb, dispersing the firing rate and latency of output action potentials to an extent that depends on the strength of the input. Thus, the presence of two types of principal cells in layer II of the piriform cortex may underlie coding strategies used for the representation of odors.

Section: Importance For Olfactory Codingmentioning

confidence: 80%

Neural Coding by Two Classes of Principal Cells in the Mouse Piriform Cortex

Suzuki

Bekkers²

2006

111

163

“…Reliability of action potential timing offers an alternative view of neuronal noise, and a range of analytical techniques have been used to measure timing variability, or jitter (for review, see Billimoria et al, 2006;Kreuz et al, 2007). The ISI distance method used here is a normalized estimate of jitter, with a value of 0 for perfect reliability and increasingly positive values as action potential timing becomes more unpredictable.…”

Section: Does Inherent Membrane Noise Limit Information Capacity?mentioning

confidence: 99%

“…Neuromodulation has also been reported to change the reliability of action potential timing (or its inverse, jitter) and thus the amount of information that can be transmitted by the neuron (Billimoria et al, 2006). Action potential timing jitter is a well known neuronal phenomenon with several possible sources (Rieke et al, 1997;Billimoria et al, 2006;Rokem et al, 2006;Kreuz et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

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GABAergic Excitation of Spider Mechanoreceptors Increases Information Capacity by Increasing Entropy Rather than Decreasing Jitter

Pfeiffer

French²

2009

Neurotransmitter chemicals excite or inhibit a range of sensory afferents and sensory pathways. These changes in firing rate or static sensitivity can also be associated with changes in dynamic sensitivity or membrane noise and thus action potential timing. We measured action potential firing produced by random mechanical stimulation of spider mechanoreceptor neurons during long-duration excitation by the GABA A agonist muscimol. Information capacity was estimated from signal-to-noise ratio by averaging responses to repeated identical stimulation sequences. Information capacity was also estimated from the coherence function between input and output signals. Entropy rate was estimated by a data compression algorithm and maximum entropy rate from the firing rate. Action potential timing variability, or jitter, was measured as normalized interspike interval distance. Muscimol increased firing rate, information capacity, and entropy rate, but jitter was unchanged. We compared these data with the effects of increasing firing rate by current injection. Our results indicate that the major increase in information capacity by neurotransmitter action arose from the increased entropy rate produced by increased firing rate, not from reduction in membrane noise and action potential jitter.

“…It has been shown in many studies that short-term synaptic plasticity plays crucial roles in configuration of neural networks for motor pattern generation (Katz and Frost, 1995;Calabrese, 1998;Katz, 1999;Sanchez and Kirk, 2000;Sakurai and Katz, 2003;Koh and Weiss, 2005;Giocomo and Hasselmo, 2007;Briggman and Kristan, 2008;Huang et al, 2008), and sensory processing (Nagai et al, 1996;Mercer, 1999;Billimoria et al, 2006;Schneggenburger and Forsythe, 2006). Previously, we suggested that the DSI transient enhancement of VSI synaptic strength serves to boost the synaptic output during the swim motor program, whereas the synaptic decrement would suppress spurious synaptic inputs made by VSI after the cessation of swimming (Sakurai and Katz, 2003).…”

Section: Functional Significance Of Timing-and State-dependent Neurommentioning

confidence: 88%

State-, Timing-, and Pattern-Dependent Neuromodulation of Synaptic Strength by a Serotonergic Interneuron

Sakurai¹,

Katz²

2009

Here we report that a serotonergic neuron evokes two distinct neuromodulatory actions with different state, timing, and firing pattern dependencies. These neuromodulatory actions may have important behavioral functions. In the mollusc, Tritonia diomedea, EPSCs evoked by ventral swim interneuron B (VSI) exhibited intrinsic plasticity; after a spike train, EPSC amplitude increased from a basal state to a potentiated state, which usually lasted Ͼ10 min. While the synapse was in a potentiated state, stimulation of a serotonergic dorsal swim interneuron (DSI) decreased VSI synaptic strength, returning it to a basal state. The extent of the DSI-evoked decrement was strongly correlated with the magnitude of the homosynaptic potentiation. This synaptic reset, or depotentiation, by DSI was blocked by the serotonin receptor antagonist methysergide and mimicked by a serotonin puff. In contrast to this state-dependent neuromodulatory action, we found that a previously described DSI-evoked transient enhancement of VSI synaptic strength was state-independent, producing the same multiplicative increase in EPSC amplitude regardless of whether the synapse was in a potentiated or basal state. These two actions also differed in their dependencies on the firing pattern of DSI and VSI action potentials. Results suggest that stateindependent synaptic enhancement by DSI may play a short-term role during a swim motor pattern, whereas state-dependent actions may have longer-lasting consequences, resetting VSI synaptic strength after a swim bout. Thus, differences in two neuromodulatory actions at one synapse may allow a serotonergic neuron to play distinct roles at different stages of a motor pattern.