scholarly journals Transient voltage-activated K+ currents in central antennal lobe neurons: cell type-specific functional properties

2017 ◽  
Vol 117 (5) ◽  
pp. 2053-2064 ◽  
Author(s):  
Lars Paeger ◽  
Viktor Bardos ◽  
Peter Kloppenburg

In this study we analyzed transient voltage-activated K+ currents ( IA) of projection neurons and local interneurons in the antennal lobe of the cockroach Periplaneta americana. The antennal lobe is the first synaptic processing station for olfactory information in insects. Local interneurons are crucial for computing olfactory information and form local synaptic connections exclusively in the antennal lobe, whereas a primary task of the projection neurons is the transfer of preprocessed olfactory information from the antennal lobe to higher order centers in the protocerebrum. The different physiological tasks of these neurons require specialized physiological and morphological neuronal phenotypes. We asked if and how the different physiological phenotypes are reflected in the functional properties of IA, which is crucial for shaping intrinsic electrophysiological properties of neurons. Whole cell patch-clamp recordings from adult male P. americana showed that all their central antennal lobe neurons can generate IA. The current exhibited marked cell type-specific differences in voltage dependence of steady-state activation and inactivation, and differences in inactivation kinetics during sustained depolarization. Pharmacological experiments revealed that IA in all neuron types was partially blocked by α-dendrotoxin and phrixotoxin-2, which are considered blockers with specificity for Shaker- and Shal-type channels, respectively. These findings suggest that IA in each cell type is a mixed current generated by channels of both families. The functional role of IA was analyzed in experiments under current clamp, in which portions of IA were blocked by α-dendrotoxin or phrixotoxin-2. These experiments showed that IA contributes significantly to the intrinsic electrophysiological properties, such as the action potential waveform and membrane excitability. NEW & NOTEWORTHY In the insect olfactory system, projection neurons and local interneurons have task-specific electrophysiological and morphological phenotypes. Voltage-activated potassium channels play a crucial role in shaping functional properties of these neurons. This study revealed marked cell type-specific differences in the biophysical properties of transient voltage-activated potassium currents in central antennal lobe neurons.

2009 ◽  
Vol 102 (5) ◽  
pp. 2834-2845 ◽  
Author(s):  
Andreas Husch ◽  
Moritz Paehler ◽  
Debora Fusca ◽  
Lars Paeger ◽  
Peter Kloppenburg

A diverse population of local interneurons (LNs) helps to process, structure, and spatially represent olfactory information in the insect antennal lobe. In Periplaneta americana, we identified two subtypes of nonspiking local interneurons (type II LNs) by their distinct morphological and intrinsic electrophysiological properties. As an important step toward a better understanding of the cellular mechanisms that mediate odor information processing, we present a detailed analysis of their distinct voltage-activated Ca2+ currents, which clearly correlated with their distinct intrinsic electrophysiological properties. Both type II LNs did not posses voltage-activated Na+ currents and apparently innervated all glomeruli including the macroglomerulus. Type IIa LNs had significant longer and thicker low-order neurites and innervated each glomerulus entirely and homogeneously, whereas type IIb LNs innervated only parts of each glomerulus. All type II LNs were broadly tuned and responded to odorants of many chemical classes with graded changes in the membrane potential. Type IIa LNs responded with odor-specific elaborate patterns of excitation that could also include “spikelets” riding on the depolarizations and periods of inhibition. In contrast, type IIb LNs responded mostly with sustained, relatively smooth depolarizations. Consistent with the strong active membrane properties of type IIa LNs versus type IIb LNs, the voltage-activated Ca2+ current of type IIa LNs activated at more hyperpolarized membrane potentials and had a larger transient component.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Houri Hintiryan ◽  
Ian Bowman ◽  
David L. Johnson ◽  
Laura Korobkova ◽  
Muye Zhu ◽  
...  

AbstractThe basolateral amygdalar complex (BLA) is implicated in behaviors ranging from fear acquisition to addiction. Optogenetic methods have enabled the association of circuit-specific functions to uniquely connected BLA cell types. Thus, a systematic and detailed connectivity profile of BLA projection neurons to inform granular, cell type-specific interrogations is warranted. Here, we apply machine-learning based computational and informatics analysis techniques to the results of circuit-tracing experiments to create a foundational, comprehensive BLA connectivity map. The analyses identify three distinct domains within the anterior BLA (BLAa) that house target-specific projection neurons with distinguishable morphological features. We identify brain-wide targets of projection neurons in the three BLAa domains, as well as in the posterior BLA, ventral BLA, posterior basomedial, and lateral amygdalar nuclei. Inputs to each nucleus also are identified via retrograde tracing. The data suggests that connectionally unique, domain-specific BLAa neurons are associated with distinct behavior networks.


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Debora Fusca ◽  
Peter Kloppenburg

Local interneurons (LNs) mediate complex interactions within the antennal lobe, the primary olfactory system of insects, and the functional analog of the vertebrate olfactory bulb. In the cockroach Periplaneta americana, as in other insects, several types of LNs with distinctive physiological and morphological properties can be defined. Here, we combined whole-cell patch-clamp recordings and Ca2+ imaging of individual LNs to analyze the role of spiking and nonspiking LNs in inter- and intraglomerular signaling during olfactory information processing. Spiking GABAergic LNs reacted to odorant stimulation with a uniform rise in [Ca2+]i in the ramifications of all innervated glomeruli. In contrast, in nonspiking LNs, glomerular Ca2+ signals were odorant specific and varied between glomeruli, resulting in distinct, glomerulus-specific tuning curves. The cell type-specific differences in Ca2+ dynamics support the idea that spiking LNs play a primary role in interglomerular signaling, while they assign nonspiking LNs an essential role in intraglomerular signaling.


2017 ◽  
Author(s):  
Niels R. Ntamati ◽  
Meaghan Creed ◽  
Christian Lüscher

AbstractNeurons in the periaqueductal gray (PAG) modulate threat responses and nociception. Activity in the ventral tegmental area (VTA) on the other hand can cause reinforcement and aversion. While in many situations these behaviors are related, the anatomical substrate of a crosstalk between the PAG and VTA remains poorly understood. Here we describe the anatomical and electrophysiological organization of the VTA-projecting PAG neurons. Using rabies-based, cell type-specific retrograde tracing, we observed that PAG to VTA projection neurons are evenly distributed along the rostro-caudal axis of the PAG, but concentrated in its posterior and ventrolateral segments. Optogenetic projection targeting demonstrated that the PAG-to-VTA pathway is predominantly excitatory and targets similar proportions of Ih-expressing VTA DA and GABA neurons. Taken together, these results set the framework for functional analysis of the interplay between PAG and VTA in the regulation of reward and aversion.


2016 ◽  
Vol 116 (3) ◽  
pp. 1261-1274 ◽  
Author(s):  
Amanda K. Kinnischtzke ◽  
Erika E. Fanselow ◽  
Daniel J. Simons

The functional role of input from the primary motor cortex (M1) to primary somatosensory cortex (S1) is unclear; one key to understanding this pathway may lie in elucidating the cell-type specific microcircuits that connect S1 and M1. Recently, we discovered that a subset of pyramidal neurons in the infragranular layers of S1 receive especially strong input from M1 (Kinnischtzke AK, Simons DJ, Fanselow EE. Cereb Cortex 24: 2237–2248, 2014), suggesting that M1 may affect specific classes of pyramidal neurons differently. Here, using combined optogenetic and retrograde labeling approaches in the mouse, we examined the strengths of M1 inputs to five classes of infragranular S1 neurons categorized by their projections to particular cortical and subcortical targets. We found that the magnitude of M1 synaptic input to S1 pyramidal neurons varies greatly depending on the projection target of the postsynaptic neuron. Of the populations examined, M1-projecting corticocortical neurons in L6 received the strongest M1 inputs, whereas ventral posterior medial nucleus-projecting corticothalamic neurons, also located in L6, received the weakest. Each population also possessed distinct intrinsic properties. The results suggest that M1 differentially engages specific classes of S1 projection neurons, thereby regulating the motor-related influence S1 exerts over subcortical structures.


Neuron ◽  
2015 ◽  
Vol 88 (2) ◽  
pp. 298-305 ◽  
Author(s):  
Tanya Sippy ◽  
Damien Lapray ◽  
Sylvain Crochet ◽  
Carl C.H. Petersen

2020 ◽  
Author(s):  
Debora Fusca ◽  
Peter Kloppenburg

AbstractLocal interneurons (LNs) mediate complex interactions within the antennal lobe, the primary olfactory system of insects, and the functional analog of the vertebrate olfactory bulb. In the cockroach Periplaneta Americana, as in other insects, several types of LNs with distinctive physiological and morphological properties can be defined. Here, we combined whole-cell patch clamp recordings and Ca2+ imaging of individual LNs to analyze the role of spiking and nonspiking LNs in inter- and intraglomerular signaling during olfactory information processing. Spiking GABAergic LNs reacted to odorant stimulation with a uniform rise in [Ca2+]i in the ramifications of all innervated glomeruli. In contrast, in nonspiking LNs, glomerular Ca2+ signals were odorant specific and varied between glomeruli, resulting in distinct, glomerulus-specific tuning curves. The cell type-specific differences in Ca2+ dynamics support the idea that spiking LNs play a primary role in interglomerular signaling, while they assign nonspiking LNs an essential role in intraglomerular signaling.


Function ◽  
2021 ◽  
Author(s):  
Tanya Sippy ◽  
Corryn Chaimowitz ◽  
Sylvain Crochet ◽  
Carl C H Petersen

Abstract The striatum integrates sensorimotor and motivational signals, likely playing a key role in reward-based learning of goal-directed behavior. However, cell type-specific mechanisms underlying reinforcement learning remain to be precisely determined. Here, we investigated changes in membrane potential dynamics of dorsolateral striatal neurons comparing naïve mice and expert mice trained to lick a reward spout in response to whisker deflection. We recorded from three distinct cell types: i) direct pathway striatonigral neurons, which express type 1 dopamine receptors; ii) indirect pathway striatopallidal neurons, which express type 2 dopamine receptors; and iii) tonically active, putative cholinergic, striatal neurons. Task learning was accompanied by cell type-specific changes in the membrane potential dynamics evoked by the whisker deflection and licking in successfully-performed trials. Both striatonigral and striatopallidal types of striatal projection neurons showed enhanced task-related depolarization across learning. Striatonigral neurons showed a prominent increase in a short latency sensory-evoked depolarization in expert compared to naïve mice. In contrast, the putative cholinergic striatal neurons developed a hyperpolarizing response across learning, driving a pause in their firing. Our results reveal cell type-specific changes in striatal membrane potential dynamics across the learning of a simple goal-directed sensorimotor transformation, helpful for furthering the understanding of the various potential roles of different basal ganglia circuits.


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