Differential expression of voltage-sensitive K+ and Ca2+ currents in neurons of the honeybee olfactory pathway

Abstract

The formation of olfactory memory is a multistage process that involves different areas of the insect brain. Olfactory conditioning of the proboscis extension reflex of the honeybee has proved to be a very powerful system for studying learningrelated neural mechanisms, enabling major neural elements of the olfactory and reward pathways in the honeybee brain to be identified (Erber et al., 1980;Hammer, 1993;Mauelshagen, 1993;Grünewald, 1999b;Hammer and Menzel, 1998) (for reviews, see Hammer, 1997;Menzel, 1999Menzel, , 2001) and several molecular pathways involved in this behaviour to be elucidated (e.g. Hildebrandt and Müller, 1995;Müller, 1996Müller, , 2000Grünbaum and Müller, 1998;Fiala et al., 1999) (for a review, see Menzel and Müller, 1996). Odors are perceived by sensillae on the honeybee antennae. The axons of the olfactory receptor neurons terminate within the primary olfactory neuropils of the honeybee brain, the antennal lobes. Olfactory information is processed here in a complex spatio-temporal fashion (Joerges et al., 1997;Stopfer et al., 1997;Sachse et al., 1999) and projection neurons transmit olfactory information from the antennal lobes to the lateral protocerebral lobes and the mushroom bodies within the protocerebrum (Homberg, 1984;Fonta et al., 1993;Abel et al., 2001). In the mushroom body calyces the projection neurons synapse onto mushroom body-intrinsic Kenyon cells, named after their discoverer (Kenyon, 1896). Olfactory information converges here with information from other sensory modalities, such as visual input in the mushroom body, and with reward-processing modulatory neurons from the suboesophageal ganglion (Erber et al., 1987;Hammer and Menzel, 1995). Intracellular recordings showed that odor applications induce complex spiking patterns in projection neurons, thus encoding olfactory and gustatory sensory information (Stopfer et al., 1997;Abel et al., 2001;Müller et al., 2002). The underlying ion channels of projection neurons have not yet been analysed, however, because the neurons could not be identified and distinguished from local interneurons, as is possible in other insects (Hayashi and Hildebrand, 1990;Oland and Hayashi, 1993

Intrinsic and Circuit Properties Favor Coincidence Detection for Decoding Oscillatory Input

“…In particular, they indicate that coincident EPSPs can summate supralinearly, favoring coincidence detection. Many of these observed subthreshold nonlinearities are likely attributable to the active conductances observed in KCs in culture (Schafer et al, 1994;Grunewald, 2003). These nonlinearities can amplify coincident EPSPs (as in the case of spikelets).…”

“…KCs and lateral horn interneurons (LHIs) (Perez-Orive et al, 2002) were modeled as a single compartment with channels governed by Hodgkin-Huxley kinetics as follows: (Sloper and Powell, 1979), and a transient (A-type) K ϩ current, I K,A (Grunewald, 2003); fast Na ϩ , I Na , and delayed rectified K ϩ , I K , currents were included to account for spike generation (Traub, 1982). Current kinetics were adjusted to 23°C.…”

“…The active conductances that have been observed in cultured KCs (Schafer et al, 1994;Grunewald, 2003) were included in a Hodgkin-Huxley type KC model (see Materials and Methods). This simple model of a KC with realistic active conductances can produce EPSP waveforms similar to those observed in vivo and demonstrates the important effect that these active properties have on the temporal window in which a neuron integrates its input.…”

The modulation of voltage-gated potassium channels by anisotonicity in trigeminal ganglion neurons

“…It is reported that more and more α subunits as well as β subunit of VGPCs have been found in rat trigeminal ganglion (TG) (Gutman et al, 2005;Rasband and Trimmer, 2006). VGPCs show significant diversity in their biophysical and pharmacologic properties and there are at least two types of VGPC currents in sensory neurons: slow-inactivating potassium current (I K ), displaying slow or sometimes incomplete inactivation and fast-inactivating potassium current (I A ) exhibiting fast inactivation kinetics (Catacuzzeno et al, 2003;Gold et al, 1996;Grunewald, 2003;Stewart et al, 2003). VGPCs participate in the action potential (AP) and determine the excitability of cells by regulating the resting membrane potential, the threshold of AP and the frequency of AP firings (Rasband and Trimmer, 2006;Yost, 1999).…”

Excitable properties of adult skeletal muscle fibres from the honeybeeApis mellifera

“…Over the last ten years, honeybee nervous system electrical activity has been studied at the cellular and molecular level with electrophysiological techniques. A number of ionic currents have been characterized, mainly in neurons from two regions of the honeybee brain: mushroom bodies and antennal lobes (Goldberg et al, 1999;Grunewald, 2003;Kloppenburg et al, In the hive, a wide range of honeybees tasks such as cell cleaning, nursing, thermogenesis, flight, foraging and inter-individual communication (waggle dance, antennal contact and trophallaxy) depend on proper muscle activity. However, whereas extensive electrophysiological studies have been undertaken over the past ten years to characterize ionic currents underlying the physiological neuronal activity in honeybee, ionic currents underlying skeletal muscle fibre activity in this insect remain, so far, unexplored.…”