Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta

Abstract

Intracellular recordings were made from the major neurites of local interneurons in the moth antennal lobe. Antennal nerve stimulation evoked 3 patterns of postsynaptic activity: (i) a short-latency compound excitatory postsynaptic potential that, based on electrical stimulation of the antennal nerve and stimulation of the antenna with odors, represents a monosynaptic input from olfactory afferent axons (71 out of 86 neurons), (ii) a delayed activation of firing in response to both electrical- and odor-driven input (11 neurons), and (iii) a delayed membrane hyperpolarization in response to antennal nerve input (4 neurons). Simultaneous intracellular recordings from a local interneuron with short-latency responses and a projection (output) neuron revealed unidirectional synaptic interactions between these two cell types. In 20% of the 30 pairs studied, spontaneous and current-induced spiking activity in a local interneuron correlated with hyperpolarization and suppression of firing in a projection neuron. No evidence for recurrent or feedback inhibition of projection neurons was found. Furthermore, suppression of firing in an inhibitory local interneuron led to an increase in firing in the normally quiescent projection neuron, suggesting that a disinhibitory pathway may mediate excitation in projection neurons. This is the first direct evidence of an inhibitory role for local interneurons in olfactory information processing in insects. Through different types of multisynaptic interactions with projection neurons, local interneurons help to generate and shape the output from olfactory glomeruli in the antennal lobe.

Inhibition of nitric oxide and soluble guanylyl cyclase signaling affects olfactory neuron activity in the moth, Manduca sexta

“…Changes in odor response onset were sometimes observed (Fig. 1f); this phenomenon could be a result in a reduction in driving force through LN inhibition (Christensen et al 1993) or changes in PN membrane properties. Thus the effects of NO on the processing of odor information are likely to be multifaceted resulting in both greater efficacy of the LN network and increased sensitivity of PNs.…”

“…Neuron activity was only analyzed if the recording could be held long enough to apply a saline wash for >4 min (many other neurons showed similar effects but could not be held long enough to wash out the drug). Neurons were identified as PNs or LNs based on previously characterized physiological responses to antennal nerve shock Christensen et al 1993Christensen et al , 1998a or morphologically from LY dye fills (below).…”

“…These inter-synaptic signaling events include the loss of synaptic inhibition provided by presynaptic LNs to PNs ( Fig. 1f; Christensen et al 1993;Lei et al 2002). Thus, NO is likely to directly affect inter-and intraglomerular LN responses to odor, which then indirectly affects post-synaptic PN responses.…”

“…Thus, NO is likely to directly affect inter-and intraglomerular LN responses to odor, which then indirectly affects post-synaptic PN responses. Disinhibitory pathways, where LNs likely synapse onto and inhibit other LNs (Waldrop et al 1987;Christensen et al 1993Christensen et al , 1998aChristensen et al , 1998b, were also compromised and likely resulted in the appearances of increased responses to odor (Fig. 2g, j) even when an individual LN was not directly affected by a loss of NO signaling (LN23 ; Table 2).…”

“…Orientation D: dorsal; L: lateral Table 1 The effects of blocking NO synthesis in antennal lobe neurons PNs in the lateral cell body cluster (LC) with projections leaving the AL via the outer cerebral tract, as deWned by Homberg et al 1988); or (2) ramiWcations (PNs MGC macroglomerular complex; all the MGC neurons had cell bodies in the MC; LNs were categorized according to Matsumoto and Hildebrand (1981): (1) Ia-LNs have a major branch leading to arborizations only to a subset of the regular, plant-speciWc glomeruli; (2) Ib-LNs have equal arborizations to most regular glomeruli; (3) IIb-LNs have equal arborizations to most regular glomeruli and the MGC). Neurons were also characterized physiologically by electrically shocking the antennal nerve (Christensen et al 1993). PN9 was categorized as MGC because of its response to pheromone.…”