Synaptic connections between GABA-immunoreactive neurons and uniglomerular projection neurons within the antennal lobe of the cockroach,Periplaneta americana

Abstract

Synapses within deutocerebral glomeruli between GABA-immunoreactive, putatively inhibitory local interneurons and uniglomerular projection (output) neurons were demonstrated by means of a combination of GABA-immunogold labeling and intracellular HRP injection. The following connections were identified. 1) GABA-immunoreactive (GABAir) neurons form output synapses in a dyadic fashion onto a uniglomerular projection neuron and, in addition, a second GABAir neuron. A uniglomerular projection neuron in turn forms dyadic output synapses onto two GABAir neurons. Several examples of reciprocal connections have been identified between, first, GABAir neurons and uniglomerular projection neurons, and, second, GABAir neurons themselves. 2) GABAir neurons are serially connected with uniglomerular projection neurons via interposed GABAir processes. In some cases, also the first GABAir process of such a polysynaptic connection formed an output synapse onto the projection neuron. Such serial connections may form the structural basis for both, the feedforward inhibition as well as the feedforward disinhibition of uniglomerular projection neurons by GABAergic neurons. The reciprocal contacts may serve as control devices that modulate the output activity of the projection neurons.

Spatio-temporal activity patterns of odor-induced synchronized potentials revealed by voltage-sensitive dye imaging and intracellular recording in the antennal lobe of the cockroach

“…All characterized local interneurons exhibited oligoglomerular projections; they had dendritic arborizations in most, but not all, glomeruli (Figures 7A–C) and their primary axons formed y-shaped branches in the AL (Figure 7C, arrowheads). These morphological features are consistent with those of GABAergic type-1 local interneurons, which make inhibitory synapse with the projection neurons (Distler et al, 1998; Husch et al, 2009b). All stained local interneurons extended neurites into the glomeruli in which synchronized potentials were evoked by enanthic acid (Figure 7B).…”

“…To identify the glomeruli in which the synchronized potentials were generated, the VSD images were superimposed on the confocal stack of images from the same AL preparation. Nine of the 12 pixels corresponded to seven glomeruli of the postero-ventral group (E03, E04, E05, E06, E07, E12, and I12 glomeruli in Figure 5C) and the remaining three pixels (numbers 10, 11, and 12 in Figure 5A) were located in the anterior soma cluster, comprising the somata of the secondary olfactory interneurons (Distler and Boeckh, 1997a,b; Distler et al, 1998). In contrast to the longer decay phases of synchronized potentials induced by citral and pentanol, the potentials induced by enanthic acid persisted for only 150–500 ms after the onset of the olfactory stimulus (Figure 5B).…”

“…Three pixels (numbers 10, 11, and 12 in Figure 5B), which recorded enanthic-acid induced synchronized potentials, corresponded to the cluster of somata of projection neurons and local interneurons (Distler and Boeckh, 1997a,b; Distler et al, 1998). In order to clarify which interneurons contributed to the synchronized potentials, we intracellularly recorded responses to enanthic acid from single projection neurons (Figure 6) and local interneurons (Figure 7) which had dendritic arborizations in the glomeruli located just beneath the anterior surface of the AL.…”

Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster

“…Thus, there are four sources of excitatory input into the glomerular circuitry: the OSNs, the uPNs, the multiglomerular eLNs (electrical synapses), and the PNs of the lateral antennal lobe tract (lALT) (Okada et al, 2009;Yaksi and Wilson, 2010). The ultrastructural demonstration reported here of the existence of PN recurrent synapses had been shown in Periplaneta (Distler et al, 1998) and Manduca (Sun et al, 1997) but was yet not confirmed in Drosophila, although it had been indicated by optical imaging (Ng et al, 2002;Pech et al, 2015) and genetic labeling (Mosca and Luo, 2014).…”

Complete identification of four giant interneurons supplying mushroom body calyces in the cockroach Periplaneta americana

“…In contrast, type 1 PNs exhibit temporally complex response patterns interposed by IPSPs (Watanabe et al, ) and those from the other 100 glomeruli provide divergent input to specific layers and/or zones in broad zones II–IIIA (Strausfeld and Li, ; Watanabe et al, ). Some degree of inhibitory gain control of type 1 uniglomerular PNs therefore already occurs in the antennal lobe in which numerous monosynaptic connections are formed between PNs and GABA‐immunoreactive LNs (Distler et al, ); hence, zones II–IIIA of the calyx appear to be more appropriate than zone I for fine discrimination of odors.…”