Mechanisms and benefits of granule cell latency coding in the mouse olfactory bulb

Giridhar, Sonya; Urban, Nathaniel N.

doi:10.3389/fncir.2012.00040

Cited by 11 publications

(11 citation statements)

References 63 publications

(98 reference statements)

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“…Kv1.3 channels drive the duration of the action potential spike train, the interspike interval (ISI), latency to the first spike, and the pause duration between spike clusters in mitral cells of the olfactory bulb (Fadool et al 2011; Mast & Fadool, 2012). Because the typical working concentration of d ‐glucose in the ASCF used to isolate the olfactory bulb and the external recording bath solutions reported for slice electrophysiological preparations of the olfactory bulb range between 10 and 22–25 m m glucose (Dong et al 2009; Ma & Lowe, 2010; Borisovska et al 2011; Lui et al 2011; Masurkar & Chen, 2011; Giridhar & Urban, 2012; Gire et al 2012), we initiated our investigation of mitral cell glucose sensitivity using the two extremes of 0 and 22 m m glucose. Regardless of the order of solution presentation, mitral cell firing frequency was found to increase or decrease in response to a change in glucose (change in spike frequency was not significantly different across solution order, 0 to 22 m m , 179.7 ± 34.6% change ( n = 6); 22 to 0 m m , 178.7 ± 27.7 ( n = 18), Student's t test, arc‐sine transformation for percentage data, α≤ 0.05).…”

Section: Resultsmentioning

confidence: 99%

“…Odour‐induced mitral/tufted cell activity significantly increases metabolic oxygen consumption (Lecoq et al 2009) and thereby requires a strong demand for glucose and related metabolic substrates. It is also interesting to note that the artificial cerebral spinal fluid used for bath solution in most olfactory bulb slice electrophysiology experiments contains anywhere from 10 to 25 m m d ‐glucose (Dong et al 2009; Ma & Lowe, 2010; Lui et al 2011; Borisovska et al 2011; Masurkar & Chen, 2011; Giridhar & Urban, 2012; Gire et al 2012). These are much higher concentrations than would ever be seen by the brain in vivo and may even act to suppress evoked action potential discharge as has been seen in a large proportion of mitral cells in our study.…”

Section: Discussionmentioning

confidence: 99%

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Glucose sensitivity of mouse olfactory bulb neurons is conveyed by a voltage‐gated potassium channel

Tucker¹,

Cho²,

Thiebaud³

et al. 2013

The Journal of Physiology

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Key points• Potassium ion channels dampen excitability of neurons but may also be sensors of internal metabolism.• Mice with gene-targeted deletion of the potassium channel Kv1.3, a channel regulating action potential spike frequency in the olfactory bulb, are 'super-smellers' and resistant to diet-induced obesity.• Electrophysiology experiments demonstrate that Kv1.3 is sensitive to the active form of glucose and that Kv1.3-expressing mitral neurons of the olfactory bulb are predominantly inhibited by a change to high glucose concentration.• Modulation of the neuron target properties of spike firing rather than action potential shape involves synaptic activity of glutamate or GABA signalling circuits, and is dependent upon Kv1.3 expression.• Given the rising incidence of metabolic disorders attributed to weight gain, changes in neuronal excitability in brain regions regulating sensory perception of food are of consequence if we are to understand the function of the brain under chronic hyperglycaemia as is typical with obesity. AbstractThe olfactory bulb has recently been proposed to serve as a metabolic sensor of internal chemistry, particularly that modified by metabolism. Because the voltage-dependent potassium channel Kv1.3 regulates a large proportion of the outward current in olfactory bulb neurons and gene-targeted deletion of the protein produces a phenotype of resistance to diet-induced obesity in mice, we hypothesized that this channel may play a role in translating energy availability into a metabolic signal. Here we explored the ability of extracellular glucose concentration to modify evoked excitability of the mitral neurons that principally regulate olfactory coding and processing of olfactory information. Using voltage-clamp electrophysiology of heterologously expressed Kv1.3 channels in HEK 293 cells, we found that Kv1.3 macroscopic currents responded to metabolically active (D-) rather than inactive (L-) glucose with a response profile that followed a bell-shaped curve. Olfactory bulb slices stimulated with varying glucose concentrations showed glucose-dependent mitral cell excitability as evaluated by current-clamp electrophysiology. While glucose could be either excitatory or inhibitory, the majority of the sampled neurons displayed a decreased firing frequency in response to elevated glucose concentration that was linked to increased latency to first spike and decreased action potential cluster length. Unlike modulation attributed to phosphorylation, glucose modulation of mitral cells was rapid, less than one minute, and was reversible within the time course of a patch recording. Moreover, we report that modulation targets properties of spike firing rather than action potential shape, K. Tucker and S. Cho contributed equally to this work. involves synaptic activity of glutamate or GABA signalling circuits, and is dependent upon Kv1.3 expression. Given the rising incidence of metabolic disorders attributed to weight gain, changes in neuronal excitability in brain regions regulating sensory per...

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Glucose sensitivity of mouse olfactory bulb neurons is conveyed by a voltage‐gated potassium channel

Tucker¹,

Cho²,

Thiebaud³

et al. 2013

The Journal of Physiology

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“…GL) differs from our previous study examining MC vs . TC response latencies to minimal glomerulus stimulation (Giridhar & Urban, ). For conciseness, we use the phrase ‘afferent‐evoked’ to refer to the activity and synaptic input of MCs and TCs arising from the combined direct monosynaptic OSN input and indirect polysynaptic ETC input (i.e.…”

Section: Methodsmentioning

confidence: 99%

“…Stimulus intensity was adjusted until all-or-nothing LLDs (either following or occluding direct monosynaptic OSN input) were reliably (ß95% success rate) evoked on each trial. These stimulus intensities and the position of the stimulation electrode (olfactory nerve layer (ONL) vs. GL) differs from our previous study examining MC vs. TC response latencies to minimal glomerulus stimulation (Giridhar & Urban, 2012). For conciseness, we use the phrase 'afferent-evoked' to refer to the activity and synaptic input of MCs and TCs arising from the combined direct monosynaptic OSN input and indirect polysynaptic ETC input (i.e.…”

Section: Electrophysiologymentioning

confidence: 99%

Greater excitability and firing irregularity of tufted cells underlies distinct afferent‐evoked activity of olfactory bulb mitral and tufted cells

Burton

Urban

2014

The Journal of Physiology

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119

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Key pointsr The two classes of principal neurons in the mammalian main olfactory bulb, mitral and tufted cells, respond with different firing latencies and rates to afferent-evoked input; how these differences in activity arise is incompletely understood.r Tufted cells receive stronger afferent-evoked excitation than mitral cells, but this difference alone is insufficient to account for the greater afferent-evoked firing in tufted versus mitral cells.r Mitral and tufted cells exhibit significant intrinsic functional differences; compared to mitral cells, tufted cells fire action potentials with shorter durations and faster afterhyperpolarizations and exhibit twofold greater firing rate-current curve gains and peak rates.r Tufted cells exhibit diverse firing modes, including tonic firing and irregular stuttering, and on average fire more irregularly than mitral cells.r Collectively, stronger afferent excitation, greater intrinsic excitability and more irregular firing in tufted cells combine to drive distinct responses of mitral and tufted cells to sensory input.Abstract Mitral and tufted cells, the two classes of principal neurons in the mammalian main olfactory bulb, exhibit morphological differences but remain widely viewed as functionally equivalent. Results from several recent studies, however, suggest that these two cell classes may encode complementary olfactory information in their distinct patterns of afferent-evoked activity. To understand how these differences in activity arise, we have performed the first systematic comparison of synaptic and intrinsic properties between mitral and tufted cells. Consistent with previous studies, we found that tufted cells fire with higher probability and rates and shorter latencies than mitral cells in response to physiological afferent stimulation. This stronger response of tufted cells could be partially attributed to synaptic differences, as tufted cells received stronger afferent-evoked excitation than mitral cells. However, differences in intrinsic excitability also contributed to the differences between mitral and tufted cell activity. Compared to mitral cells, tufted cells exhibited twofold greater excitability and peak instantaneous firing rates. These differences in excitability probably arise from differential expression of voltage-gated potassium currents, as tufted cells exhibited faster action potential repolarization and afterhyperpolarizations than mitral cells. Surprisingly, mitral and tufted cells also showed firing mode differences. While both cell classes exhibited regular firing and irregular stuttering of action potential clusters, tufted cells demonstrated a greater propensity to stutter than mitral cells. Collectively, stronger afferent-evoked excitation, greater intrinsic excitability and more irregular firing in tufted cells can combine to drive distinct responses of mitral and tufted cells to afferent-evoked input.

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“…Granule cells provide feedback inhibition to MTs through a reciprocal dendrodendritic synapse 21–23 . Therefore, it has been widely proposed that feedback inhibition from GCs contributes to temporally patterned activity and stimulus selectivity of MTs 24–27 . Yet, in vivo recordings from GCs have been limited to anesthetized animals 16, 28–30 .…”

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confidence: 99%

Broadly tuned and respiration-independent inhibition in the olfactory bulb of awake mice

Cazakoff

Lau

Crump

et al. 2014

Preprint

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Olfactory representations are shaped by both brain state and respiration; however, the interaction and circuit substrates of these influences are poorly understood. Granule cells (GCs) in the main olfactory bulb (MOB) are presumed to sculpt activity that reaches the olfactory cortex via inhibition of mitral/tufted cells (MTs). GCs may potentially sparsen ensemble activity by facilitating lateral inhibition among MTs, and/or they may enforce temporally-precise activity locked to breathing. Yet, the selectivity and temporal structure of GC activity during wakefulness are unknown. We recorded GCs in the MOB of anesthetized and awake mice and reveal pronounced state-dependent features of odor coding and temporal patterning. Under anesthesia, GCs exhibit sparse activity and are strongly and synchronously coupled to the respiratory cycle. Upon waking, GCs desynchronize, broaden their odor responses, and typically fire without regard for the respiratory rhythm. Thus during wakefulness, GCs exhibit stronger odor responses with less temporal structure. Based on these observations, we propose that during wakefulness GCs likely predominantly shape MT odor responses through broadened lateral interactions rather than respiratory synchronization.

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Mechanisms and benefits of granule cell latency coding in the mouse olfactory bulb

Cited by 11 publications

References 63 publications

Glucose sensitivity of mouse olfactory bulb neurons is conveyed by a voltage‐gated potassium channel

Glucose sensitivity of mouse olfactory bulb neurons is conveyed by a voltage‐gated potassium channel

Greater excitability and firing irregularity of tufted cells underlies distinct afferent‐evoked activity of olfactory bulb mitral and tufted cells

Broadly tuned and respiration-independent inhibition in the olfactory bulb of awake mice

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