In-situ recording of ionic currents in projection neurons and Kenyon cells in the olfactory pathway of the honeybee

Abstract

The honeybee olfactory pathway comprises an intriguing pattern of convergence and divergence: ~60.000 olfactory sensory neurons (OSN) convey olfactory information on ~900 projection neurons (PN) in the antennal lobe (AL). To transmit this information reliably, PNs employ relatively high spiking frequencies with complex patterns. PNs project via a dual olfactory pathway to the mushroom bodies (MB). This pathway comprises the medial (m-ALT) and the lateral antennal lobe tract (l-ALT). PNs from both tracts transmit information from a wide range of similar odors, but with distinct differences in coding properties. In the MBs, PNs form synapses with many Kenyon cells (KC) that encode odors in a spatially and temporally sparse way. The transformation from complex information coding to sparse coding is a well-known phenomenon in insect olfactory coding. Intrinsic neuronal properties as well as GABAergic inhibition are thought to contribute to this change in odor representation. In the present study, we identified intrinsic neuronal properties promoting coding differences between PNs and KCs using in-situ patch-clamp recordings in the intact brain. We found very prominent K+ currents in KCs clearly differing from the PN currents. This suggests that odor coding differences between PNs and KCs may be caused by differences in their specific ion channel properties. Comparison of ionic currents of m- and l-ALT PNs did not reveal any differences at a qualitative level.

Calcium in Kenyon Cell Somata as a Substrate for an Olfactory Sensory Memory in Drosophila

“…These low voltage-activated, inward Ca 2+ currents could lead to a nonlinear Ca 2+ increase in response to odorant-induced post-synaptic potentials, and the duration of the post-odor Ca 2+ response might reflect the time required to restore baseline Ca 2+ concentrations by Ca 2+ buffers and pumps. The high voltage-activated Ca 2+ -dependent repolarizing currents could mediate the typical fast adaptation of KC spike responses to odorants ( Ito et al, 2008 ; Turner et al, 2008 ; Demmer and Kloppenburg, 2009 ; Palmer et al, 2013 ; Saha et al, 2013 ; Gupta and Stopfer, 2014 ; Kropf and Rössler, 2018 ). Indeed, in a modeling study, Betkiewicz et al (2017) predicted that odorant-induced prolonged Ca 2+ responses exist in KCs, and they suggested that the prolonged Ca 2+ -dependent repolarizing currents mediate adaptation and encode a sensory short-term memory for odorants in KCs.…”

Analysis of Synaptic Microcircuits in the Mushroom Bodies of the Honeybee

“…Physiological recordings from KCs, so far, have been mostly limited to the calcium imaging of spatial activation patterns, which has revealed important insights into experience-related changes in spatial activation patterns of pre-and postsynaptic elements in MB-calyx MG [21,23,112]. In situ electrophysiological recordings from KCs have shown that their highly phasic (sparse) temporal coding properties are most probably caused by intrinsic ion channel properties [113,114]. However, in situ patch-clamp recordings from individual KC somata are extremely difficult to obtain in the honeybee, mostly due to their small size and limited accessibility.…”

Randomly weighted receptor inputs can explain the large diversity of colour-coding neurons in the bee visual system

“…If so, the columnar, retinotopically arranged transmedullary cells might already show colour opponency and other diverse wavelength dependent response; then, they will provide more varied input to third order cells than we assumed in the current model. Lateral inhibition between third order neurons, on the other hand, may offer an alternative to variable intrinsic neuronal properties 75 as an explanation of thresholding effect in our model (as lateralization and thresholding of activation functions are theoretically analogous for the purpose of efficient neural representation 76–78 ). Whether transmedullary cells do or do not alter the spectral properties of the signal will have to remain an open question until electrophysiological experiments explicitly test their spectral response profile.…”