Odor processing in the cockroach antennal lobe-the network components

Abstract

Highly interconnected neural networks perform olfactory signal processing in the central nervous system. In insects, the first synaptic processing of the olfactory input from the antennae occurs in the antennal lobe, the functional equivalent of the olfactory bulb in vertebrates. Key components of the olfactory network in the antennal lobe are two main types of neurons: the local interneurons and the projection (output) neurons. Both neuron types have different physiological tasks during olfactory processing, which accordingly require specialized functional phenotypes. This review gives an overview of important cell type-specific functional properties of the different types of projection neurons and local interneurons in the antennal lobe of the cockroach Periplaneta americana, which is an experimental system that has elucidated many important biophysical and cellular bases of intrinsic physiological properties of these neurons.

Keywords: Antennal lobe; Local interneurons; Olfaction; Periplaneta americana; Projection neurons.

Fig. 1

Schematic illustration of the pathways from the periphery to higher brain centers in the protocerebrum. OSNs of perforated basiconic sensilla (green) run through antennal tracts T1-T4 and terminate in the n-anteroventral group of glomeruli. PNs with dendrites in these glomeruli project through the mALT to the protocerebrum. OSNs in trichoid and grooved basiconic sensilla (yellow) run through antennal tracts T5 and T6-10, respectively, and terminate in the n-posterodorsal group of glomeruli. PNs with dendrites in these glomeruli project through the mlALT II to the protocerebrum (Malun et al. ; Watanabe et al. 2012, 2017). L lateral, mALT medial antennal lobe tract, MG macroglomerulus, mlALT II mediolateral antennal lobe tract, NA n-anterior, T1-10 antennal tracts 1–10

Fig. 2

Schematic drawing of the five antennal lobe tracts that connect the antennal lobe and the protocerebrum. Courses of the tracts after (Malun et al. 1993). CA calyx, dr dorsal root, L lateral, lALT lateral antennal lobe tracts, LH lateral horn, mALT medial antennal lobe tract, mlALT II-IV mediolateral antennal lobe tract II-IV, vr ventral root

Fig. 3

Inventory of antennal lobe projection neurons (PNs). Properties were described in (Malun et al. ; Strausfeld and Li ; Watanabe et al. , ; Nishino et al. 2018). Numbers are estimated as follows: ~ 250 PN axons were counted in different antennal lobe tracts (Boeckh et al. ; Malun et al. 1993). Watanabe et al. (2010) counted ~ 205 glomeruli in the antennal lobe of P. americana, ~ 108 n-anteroventral glomeruli, which are innervated by type 2 uPNs, and ~ 97 n-posterodorsal glomeruli which are innervated by type 1 PNs. According to the one uPN per glomerulus rule, these numbers correspond to the numbers of regular uPNs. Together with the 12 uPNs innervating the macroglomerular complex (Nishino et al. 2018), it adds up to ~ 217 uPNs, which leaves ~ 33 neurons with axons in antennal lobe tracts that consequently belong to mPNs. (l/m)ALT, (lateral/medial) antennal lobe tract; MG, macroglomerulus; (m/u)PN, (multiglomerular/uniglomerular) projection neuron; (L/M/S)-PN, (large-/medium-/small-sized) receptive field macroglomerular projection neuron

Fig. 4

Inventory of the antennal lobe neurons with somata in the ventrolateral somata group (VSG). Data are summarized from the following sources: Morphological and physiological properties: (Ernst and Boeckh ; Boeckh et al. ; Husch et al. 2009a, b). Transmitter- and peptide content: (Neupert et al. , ; Fusca et al. 2013, 2015). Odor responses: Overlays of three repetitive stimulations with the same odorant (Husch et al. 2009a, b). Numbers are estimated as follows: The VSG comprises ~ 500 neurons (Ernst and Boeckh 1983), of which ~ 250 belong to PNs with axons in different antennal lobe tracts (Boeckh et al. ; Malun et al. 1993). Accordingly, ~ 250 somata of the VSG belong to LNs. Fusca et al. (2015) counted ~ 300 ChAT-lir neurons that were grouped in several clusters and ~ 100 GABA-lir somata in the region were predominantly type I LNs are located. According to Husch et al. (2009a), all type I LNs are GABA-lir, and Distler (1989) stated that the great majority of GABA-lir somata in the VSG belong to LNs, while only a marginal portion of the axons in the antennal lobe tracts are GABA-lir. In summary, there are ~ 100 GABA-lir type I LNs, and if the majority of PNs (~ 250) are ChAT-lir, of the ~ 300 ChAT-lir somata ~ 50 belong to type IIa1 LNs (Fusca et al. 2013). AL antennal lobe, AST-A allatostatin-A, AT allatotropin, ChAT choline acetyltransferase, L lateral, LH lateral horn, LN I(II) type I(II) local interneuron, mALT medial antennal lobe tract, MB mushroom body, NA n-anterior, TKRPs tachykinin-related peptides, uPN uniglomerular projection neurons. Images: Orientation applies to all images. Positions of lacking somata are marked by asterisks. Scale bars, 100 µm. Original figures from Husch et al. (2009a, b)

Fig. 5

Ca²⁺ currents (I_Ca) from uPNs, type I LNs and type II LNs. a, b Steady-state activation of I_Ca in uPNs, type I LNs, and type IIa and IIb LNs. Original traces (a) and current–voltage relations (b). The inset shows the relative current amplitudes, normalized to the maximum current of each cell type. c, d Tail currents of I_Ca (I_{Ca, tail}). Original traces (c) and current-voltage relations of normalized tail currents (d). Before averaging, the tail currents were normalized to the maximum tail current amplitude of each cell. Curves were fit to a first-order Boltzmann equation. The inset shows the quantitative comparison of voltages for half-maximal activation. Original figures from Husch et al. (2009a, b)

Fig. 6

Overview of GABA-, ChAT-, AT-, and TKRP-like immunoreactive (-lir) somata in the ventrolateral somata group (VSG). a Numbers of immunoreactive somata for the respective transmitters and modulators. b Schematic illustration of a P. americana antennal lobe, including the VSG. c Higher magnification of the to demonstrate the somata positions of the different AL neuron types. d–g Position and immunoreactivity of type I LN somata. h–k Position and immunoreactivity of type II LN somata. GABA-lir somata are indicated in green, ChAT-lir somata are indicated in pink. Yellow bands indicate allatotropin-lir somata, cyan bands indicate TKRP-lir somata. AN antennal nerve, AT allatotropin, ChAT choline acetyltransferase, L lateral, LN I type I local interneurons, LN II type II local interneurons, NA n-anterior, PC protocerebrum, TKRPs tachykinin-related peptides, uPN uniglomerular projection neurons. Original figure from Fusca et al. (2015)