Regeneration of cercal filiform hair sensory neurons in the first‐instar cockroach restores escape behavior

Abstract

Neural regeneration in the escape circuit of the first-instar cockroach is described using behavioral analysis, electrophysiology, intracellular staining, and electron microscopy. Each of the two filiform hairs on each of the animal's cerci is innervated by a single sensory neuron, which specifically synapses with a set of giant interneurons (GIs) in the terminal ganglion. These trigger a directed escape run. Severing the sensory axons causes them to degenerate and perturbs escape behavior, which is restored to near normal after 4-6 days. Within this time, afferents regenerate and reestablish arborizations in the terminal ganglion. In most cases, regenerating afferents enter the cercal glomerulus and re-form most of the specific monosynaptic connections they acquired during embryogenesis, although their morphology deviates markedly from normal; these animals reestablish near normal escape behavior. In a few cases, regenerating afferents remain within the cercus or bypass the cercal glomerulus, and thereby fail to re-form synapses with GIs; these animals continue to exhibit perturbed escape behavior. We conclude that in most cases, specific synapses are reestablished and appropriate escape behavior is restored. This regeneration system therefore provides a tractable model for the establishment of synaptic specificity in a simple neuronal circuit.

Transcriptional Control of Behavior: Engrailed Knock-Out Changes Cockroach Escape Trajectories

“…The overall pattern of escape behavior shown in these plots is similar to that of other published data on early nymphs (Dagan and Volman, 1982; Stern et al, 1997), although the proportion of “towards” turns in the control groups is somewhat lower than in previous studies. This may be due, at least in part, to the way in which wind stimuli were presented.…”

“…The wind stimulus was delivered through a 6mm diameter tube positioned 10 mm above the arena floor at an angle of 45° to the horizontal, using a modified smaller version of the loudspeaker-cone driven wind-stimulus machine previously described (Stern et al, 1997). Peak wind velocity of the stimuli was approximately 0.1 ms -1 as measured using a miniature hot wire anemometer.…”

Regeneration of olfactory afferent axons in the locust brain

“…In the more easily accessible insect PNS, regeneration has been studied in cockroach motor neurons (Denburg et al,1977; Whitington,1979) and in the cercal system of crickets (Roederer and Cohen,1983; Chiba and Murphey,1991) and cockroaches (Stern et al,1997). Extensive studies have been carried out on regeneration in the auditory system of crickets (Pallas and Hoy,1986), bush crickets (Krüger et al,2010), and grasshoppers (Lakes and Kalmring,1991; Lakes‐Harlan and Pfahlert,1995; Jacobs and Lakes‐Harlan,1999; Ostrowski et al,2011), which involved functional recovery on both electrophysiological and behavioral levels.…”

Regeneration in the auditory system of nymphal and adult bush crickets Tettigonia viridissima

“…6B). Previous studies show that synapses can be rebuilt in regeneration processes in orthopterans (Killian et al , 1983; Lakes et al , 1990; Lakes & Kalmring, 1991; Jacobs & Lakes‐Harlan, 2000) and a restoration of synaptic connections is demonstrated in the afferent cercal systems of crickets and cockroaches (Chiba & Murphey, 1991; Stern et al , 1997).…”

“…Auditory interneurones ipsilateral to the crushing side lose their responses to sensory stimulation immediately after crushing, which is a common result of injury to afferents (Lakes et al , 1990; Lakes‐Harlan & Pfahlert, 1995; Stern et al , 1997). In adult T. viridissima , responses in the connective ipsilateral to the crush are found after 10 days (Fig.…”