Monoaminergic modulation of the ionic channels in Kenyon cells isolated from the mushroom body of the cricket brain

AbstractOlfactory learning and conditioning in the fruit fly is typically modelled by correlation-based associative synaptic plasticity. It was shown that the conditioning of an odor-evoked response by a shock depends on the connections from Kenyon cells (KC) to mushroom body output neurons (MBONs). Although on the behavioral level conditioning is recognized to be predictive, it remains unclear how MBONs form predictions of aversive or appetitive values (valences) of odors on the circuit level. We present behavioral experiments that are not well explained by associative plasticity between conditioned and unconditioned stimuli, and we suggest two alternative models for how predictions can be formed. In error-driven predictive plasticity, dopaminergic neurons (DANs) represent the error between the predictive odor value and the shock strength. In target-driven predictive plasticity, the DANs represent the target for the predictive MBON activity. Predictive plasticity in KC-to-MBON synapses can also explain trace-conditioning, the valence-dependent sign switch in plasticity, and the observed novelty-familiarity representation. The model offers a framework to dissect MBON circuits and interpret DAN activity during olfactory learning.

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Taurine-, aspartate- and glutamate-like immunoreactivity identifies chemically distinct subdivisions of Kenyon cells in the cockroach mushroom body

The Journal of Comparative Neurology ◽

10.1002/cne.1355 ◽

2001 ◽

Vol 439 (3) ◽

pp. 352-367 ◽

Cited By ~ 54

Author(s):

Irina Sinakevitch ◽

Sarah M. Farris ◽

Nicholas J. Strausfeld

Keyword(s):

Mushroom Body ◽

Kenyon Cells

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I A in Kenyon Cells of the Mushroom Body of Honeybees Resembles Shaker Currents: Kinetics, Modulation by K+, and Simulation

Journal of Neurophysiology ◽

10.1152/jn.1999.81.4.1749 ◽

1999 ◽

Vol 81 (4) ◽

pp. 1749-1759 ◽

Cited By ~ 24

Author(s):

Corinna Pelz ◽

Johannes Jander ◽

Hendrik Rosenboom ◽

Martin Hammer ◽

Randolf Menzel

Keyword(s):

Action Potential ◽

Time Constant ◽

Mushroom Body ◽

Delayed Rectifier ◽

Patch Clamp Technique ◽

Time Constants ◽

Voltage Gated ◽

Kenyon Cells ◽

Recovery From Inactivation ◽

A Current

I A in Kenyon cells of the mushroom body of honeybees resembles shaker currents: kinetics, modulation by K+, and simulation. Cultured Kenyon cells from the mushroom body of the honeybee, Apis mellifera, show a voltage-gated, fast transient K+ current that is sensitive to 4-aminopyridine, an A current. The kinetic properties of this A current and its modulation by extracellular K+ ions were investigated in vitro with the whole cell patch-clamp technique. The A current was isolated from other voltage-gated currents either pharmacologically or with suitable voltage-clamp protocols. Hodgkin- and Huxley-style mathematical equations were used for the description of this current and for the simulation of action potentials in a Kenyon cell model. Activation and inactivation of the A current are fast and voltage dependent with time constants of 0.4 ± 0.1 ms (means ± SE) at +45 mV and 3.0 ± 1.6 ms at +45 mV, respectively. The pronounced voltage dependence of the inactivation kinetics indicates that at least a part of this current of the honeybee Kenyon cells is a shaker-like current. Deactivation and recovery from inactivation also show voltage dependency. The time constant of deactivation has a value of 0.4 ± 0.1 ms at −75 mV. Recovery from inactivation needs a double-exponential function to be fitted adequately; the resulting time constants are 18 ± 3.1 ms for the fast and 745 ± 107 ms for the slow process at −75 mV. Half-maximal activation of the A current occurs at −0.7 ± 2.9 mV, and half-maximal inactivation occurs at −54.7 ± 2.4 mV. An increase in the extracellular K+concentration increases the conductance and accelerates the recovery from inactivation of the A current, affecting the slow but not the fast time constant. With respect to these modulations the current under investigation resembles some of the shaker-like currents. The data of the A current were incorporated into a reduced computational model of the voltage-gated currents of Kenyon cells. In addition, the model contained a delayed rectifier K+ current, a Na+current, and a leakage current. The model is able to generate an action potential on current injection. The model predicts that the A current causes repolarization of the action potential but not a delay in the initiation of the action potential. It further predicts that the activation of the delayed rectifier K+ current is too slow to contribute markedly to repolarization during a single action potential. Because of its fast activation, the A current reduces the amplitude of the net depolarizing current and thus reduces the peak amplitude and the duration of the action potential.

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Current- and Voltage-Clamp Recordings and Computer Simulations of Kenyon Cells in the Honeybee

Journal of Neurophysiology ◽

10.1152/jn.01259.2003 ◽

2004 ◽

Vol 92 (4) ◽

pp. 2589-2603 ◽

Cited By ~ 43

Author(s):

Daniel G. Wüstenberg ◽

Milena Boytcheva ◽

Bernd Grünewald ◽

John H. Byrne ◽

Randolf Menzel ◽

...

Keyword(s):

Voltage Clamp ◽

Mushroom Body ◽

Outward Current ◽

Delayed Rectifier ◽

Transient Outward Current ◽

Insect Brain ◽

Type Model ◽

Kenyon Cells ◽

Fast Transient

The mushroom body of the insect brain is an important locus for olfactory information processing and associative learning. The present study investigated the biophysical properties of Kenyon cells, which form the mushroom body. Current- and voltage-clamp analyses were performed on cultured Kenyon cells from honeybees. Current-clamp analyses indicated that Kenyon cells did not spike spontaneously in vitro. However, spikes could be elicited by current injection in approximately 85% of the cells. Of the cells that produced spikes during a 1-s depolarizing current pulse, approximately 60% exhibited repetitive spiking, whereas the remaining approximately 40% fired a single spike. Cells that spiked repetitively showed little frequency adaptation. However, spikes consistently became broader and smaller during repetitive activity. Voltage-clamp analyses characterized a fast transient Na+ current ( INa), a delayed rectifier K+ current ( IK,V), and a fast transient K+ current ( IK,A). Using the neurosimulator SNNAP, a Hodgkin–Huxley-type model was developed and used to investigate the roles of the different currents during spiking. The model led to the prediction of a slow transient outward current ( IK,ST) that was subsequently identified by reevaluating the voltage-clamp data. Simulations indicated that the primary currents that underlie spiking are INa and IK,V, whereas IK,A and IK,ST primarily determined the responsiveness of the model to stimuli such as constant or oscillatory injections of current.

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Cultured Insect Mushroom Body Neurons Express Functional Receptors for Acetylcholine, GABA, Glutamate, Octopamine, and Dopamine

Journal of Neurophysiology ◽

10.1152/jn.1999.81.1.1 ◽

1999 ◽

Vol 81 (1) ◽

pp. 1-14 ◽

Cited By ~ 55

Author(s):

M. Cayre ◽

S. D. Buckingham ◽

S. Yagodin ◽

D. B. Sattelle

Keyword(s):

Patch Clamp ◽

Mushroom Body ◽

Gaba Receptor ◽

Time Course ◽

Reversal Potential ◽

Acheta Domesticus ◽

Free Calcium ◽

Kenyon Cells ◽

Inward Currents ◽

Patch Clamp Electrophysiology

Cayre, M., S. D. Buckingham, S. Yagodin, and D. B. Sattelle. Cultured insect mushroom body neurons express functional receptors for acetylcholine, GABA, glutamate, octopamine, and dopamine. J. Neurophysiol. 81: 1–14, 1999. Fluorescence calcium imaging with fura-2 and whole cell, patch-clamp electrophysiology was applied to cultured Kenyon cells (interneurons) isolated from the mushroom bodies of adult crickets ( Acheta domesticus) to demonstrate the presence of functional neurotransmitter receptors. In all cells investigated, 5 μM acetylcholine (ACh, n = 52) evoked an increase in intracellular free calcium ([Ca2+]i). Similar effects were observed in response to 10 μM nicotine. The ACh response was insensitive to atropine (50 μM) but was reduced by mecamylamine (50 μM) and α-bungarotoxin (α-bgt, 10 μM). ACh-induced inward ion currents ( n = 28, E ACh ∼0 mV) were also blocked by 1 μM mecamylamine and by 1 μM α-bgt. Nicotine-induced inward currents desensitized more rapidly than ACh responses. Thus functional α-bgt–sensitive nicotinic ACh receptors are abundant on all Kenyon cells tested, and their activation leads to an increase in [Ca2+]i. γ-Aminobutyric acid (GABA, 100 μM) triggered a sustained decrease in [Ca2+]i. Similar responses were seen with a GABAA agonist, muscimol (100 μM), and a GABAB agonist, 3-APPA (1 mM), suggesting that more than one type of GABA receptor can affect [Ca2+]i. This action of GABA was not observed when the extracellular KCl concentration was lowered. All cells tested ( n = 26) with patch-clamp electrophysiology showed picrotoxinin (PTX)-sensitive, GABA-induced (30–100 μM) currents with a chloride-sensitive reversal potential. Thus, an ionotropic PTX-sensitive GABA receptor was found on all Kenyon cells tested. Most (61%) of the 54 cells studied responded to l-glutamate (100 μM) application either with a biphasic increase in [Ca2+]i or with a single, delayed, sustained [Ca2+]i increase. Nearly all cells tested (95%, n = 19) responded to (100 μM) l-glutamate with rapidly desensitizing, inward currents that reversed at approximately −30 mV. Dopamine (100 μM) elicited either a rapid or a delayed increase in [Ca2+]i in 63% of the 26 cells tested. The time course of these responses varied greatly among cells. Dopamine failed to elicit currents in patch-clamped cells ( n = 4). A brief decrease in [Ca2+]i was induced by octopamine (100 μM) in ∼54% of the cells tested ( n = 35). However, when extracellular CaCl2 was lowered, octopamine triggered a substantial increase in [Ca2+]i in 35% of the cells tested ( n = 26). No octopamine-elicited currents were detected in patched-clamped cells ( n = 10).

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