Phasic Stimuli Evoke Precisely Timed Spikes in Intermittently Discharging Mitral Cells

Balu, Ramani; Larimer, Phillip; Strowbridge, Ben W.

doi:10.1152/jn.00016.2004

Cited by 118 publications

(184 citation statements)

References 59 publications

(78 reference statements)

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“…That is, the better a neuron encodes a stimulus, the faster it will be in responding to it. This temporal dependence is well supported by empirical data (Sobotka & Ringo, 1996;James & Gauthier, 2006;Balu, Larimer, & Strowbridge, 2004). Figure 4 shows the condition when lateral inhibition is implemented in the network.…”

Section: Resultssupporting

confidence: 71%

Dissociable Forms of Repetition Priming: A Computational Model

Makukhin

Bolland

2014

Neural Computation

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Nondeclarative memory and novelty processing in the brain is an actively studied field of neuroscience, and reducing neural activity with repetition of a stimulus (repetition suppression) is a commonly observed phenomenon. Recent findings of an opposite trend-specifically, rising activity for unfamiliar stimuli-question the generality of repetition suppression and stir debate over the underlying neural mechanisms. This letter introduces a theory and computational model that extend existing theories and suggests that both trends are, in principle, the rising and falling parts of an inverted U-shaped dependence of activity with respect to stimulus novelty that may naturally emerge in a neural network with Hebbian learning and lateral inhibition. We further demonstrate that the proposed model is sufficient for the simulation of dissociable forms of repetition priming using real-world stimuli. The results of our simulation also suggest that the novelty of stimuli used in neuroscientific research must be assessed in a particularly cautious way. The potential importance of the inverted-U in stimulus processing and its relationship to the acquisition of knowledge and competencies in humans is also discussed.

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Section: Resultssupporting

confidence: 71%

Dissociable Forms of Repetition Priming: A Computational Model

Makukhin

Bolland

2014

Neural Computation

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“…Mitral cells show a characteristic prolonged subthreshold period after depolarizing steps; often the initial response is dominated by smallamplitude membrane potential oscillations before the first cluster of action potentials is generated (Balu et al 2004;Chen and Shepherd 1997;Desmaisons et al 1999). In addition to blocking fast sodium-channel-dependent action potentials, TTX attenuated the sustained subthreshold depolarization and blocked subthreshold membrane potential oscillations ( Fig.…”

Section: R E S U L T Smentioning

confidence: 99%

“…In some experiments, a current injection waveform consisting of a train of four temporally overlapping EPSP-like waveforms was injected into mitral cells (Balu et al 2004;Halabisky and Strowbridge 2003). Each simulated EPSP in the train was generated using a single alpha function with a decay time constant of 80 ms.…”

Section: Data Acquisition and Analysismentioning

confidence: 99%

Opposing Inward and Outward Conductances Regulate Rebound Discharges in Olfactory Mitral Cells

Balu¹,

Strowbridge

2007

Journal of Neurophysiology

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Balu R, Strowbridge BW. Opposing inward and outward conductances regulate rebound discharges in olfactory mitral cells. J Neurophysiol 97: 1959Neurophysiol 97: -1968Neurophysiol 97: , 2007. First published December 6, 2006; doi:10.1152/jn.01115.2006. The olfactory bulb, a second-order sensory brain region, relays afferent input from olfactory receptor neurons to piriform cortex and other higher brain centers. Although large inhibitory postsynaptic potentials (IPSPs) are evident in in vivo intracellular recordings from mitral cells, the functional significance of these synaptic responses has not been defined. In many brain regions, IPSPs can function to either inhibit spiking by transiently suppressing activity or can evoke spiking directly by triggering rebound discharges. We used whole cell patch-clamp recordings from mitral cells in olfactory bulb slices to investigate the mechanisms by which IPSPs regulate mitral cell spike discharges. Mitral cells have unusual intrinsic membrane properties that support rebound spike generation in response to small-amplitude (3-5 mV) but not largeamplitude hyperpolarizing current injections or IPSPs. Rebound spiking occurring in mitral cells was dependent on recovery of subthreshold Na currents, and could be blocked by tetrodotoxin (TTX, 1 M) or the subthreshold Na channel blocker riluzole (10 M). Surprisingly, larger-amplitude hyperpolarizing stimuli impeded spike generation by recruiting a transient outward I A -like current that was sensitive to high concentrations of 4-aminopyridine and Ba. The interplay of voltage-gated subthreshold Na channels and transient outward current produces a narrow range of IPSP amplitudes that generates rebound spikes. We also found that subthreshold Na channels boost subthreshold excitatory stimuli to produce membrane voltages where granule-cell-mediated IPSPs can produce rebound spikes. These results demonstrate how the intrinsic membrane properties of mitral cells enable inhibitory inputs to bidirectionally control spike output from the olfactory bulb.

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“…In the olfactory bulb, these channels are expressed predominantly by granule cells and periglomerular cells rather than in mitral cells (Serodio and Rudy, 1998). Other transient potassium currents (such as the D-current, expressed by mitral cells) are blocked by much lower concentrations of 4-AP (nanomolar range) (Balu et al, 2004).…”

Section: Asynchrony Of Granule Cell Activation Can Be Reduced By Blocmentioning

confidence: 99%

Glomerulus-Specific, Long-Latency Activity in the Olfactory Bulb Granule Cell Network

Kapoor

Urban

2006

J. Neurosci.

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Reliable, stimulus-specific temporal patterns of action potentials have been proposed to encode information in many brain areas, perhaps most notably in the olfactory system. Analysis of such temporal coding has focused almost exclusively on excitatory neurons. Thus, the role of networks of inhibitory interneurons in establishing and maintaining this reliability is unclear. Here we use imaging of population activity in vitro to investigate the mechanisms of temporal pattern generation in mouse olfactory bulb inhibitory interneurons. We show that activity of these interneurons evolves slowly in time but that individual neurons fire at reliable times, with a timescale similar to the slow changes in the patterns of odor-evoked activity and to odor discrimination. Most strikingly, the latency of a single granule cell is highly reliable from trial to trial during repeated stimulation of the same glomerulus, whereas this same cell will have a markedly different latency when a different glomerulus is activated. These data suggest that the timing of granule cell-mediated inhibition in the olfactory bulb is tightly regulated by the source of input and that inhibition may contribute to the generation of reliable temporal patterns of mitral cell activity.

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Phasic Stimuli Evoke Precisely Timed Spikes in Intermittently Discharging Mitral Cells

Cited by 118 publications

References 59 publications

Dissociable Forms of Repetition Priming: A Computational Model

Dissociable Forms of Repetition Priming: A Computational Model

Opposing Inward and Outward Conductances Regulate Rebound Discharges in Olfactory Mitral Cells

Glomerulus-Specific, Long-Latency Activity in the Olfactory Bulb Granule Cell Network

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