Ectopic sensory neurons in mutant cockroaches compete with normal cells for central targets

Development ◽  
1992 ◽  
Vol 115 (3) ◽  
pp. 773-784
Author(s):  
J.P. Bacon ◽  
J.M. Blagburn

The cercus of the first instar cockroach, Periplaneta americana, bears two filiform hairs, lateral (L) and medial (M), each of which is innervated by a single sensory neuron. These project into the terminal ganglion of the CNS where they make synaptic connections with a number of ascending interneurons. We have discovered mutant animals that have more hairs on the cercus; the most typical phenotype, called “Space Invader” (SI), has an extra filiform hair in a proximo-lateral position on one of the cerci. The afferent neuron of this supernumerary hair (SIN) “invades the space” occupied by L in the CNS and makes similar synaptic connections to giant interneurons (GIs). SIN and L compete for these synaptic targets: the size of the L EPSP in a target interneuron GI3 is significantly reduced in the presence of SIN. Morphometric analysis of the L afferent in the presence or absence of SIN shows no anatomical concomitant of competition. Ablation of L afferent allows SIN to increase the size of its synaptic input to GI3. Less frequently in the mutant population, we find animals with a supernumerary medical (SuM) sensillum. Its afferent projects to the same neuropilar region as the M afferent, makes the same set of synaptic connections to GIs, and competes with M for these synaptic targets. The study of these competitive interactions between identified afferents and identified target interneurons reveals some of the dynamic processes that go on in normal development to shape the nervous system.


1997 ◽  
Vol 33 (4) ◽  
pp. 439-458 ◽  
Author(s):  
Michael Stern ◽  
Vernita L. Ediger ◽  
Charles R. Gibbon ◽  
Jonathan M. Blagburn ◽  
Jonathan P. Bacon


1987 ◽  
Vol 127 (1) ◽  
pp. 135-157 ◽  
Author(s):  
JONATHAN M. BLAGBURN ◽  
DAVID B. SATTELLE

Intracellular microelectrodes were used to study presynaptic inhibition at a cholinergic synapse between identified neurones: the lateral filiform hair sensory neurone (LFHSN) and giant interneurone 3 (GI3) in the terminal ganglion of the first instar cockroach Periplaneta americana. The LFHSN-GI3 synapse was shown to fulfil physiological criteria for monosynaptic transmission: the latency of the EPSPs was 1.4 ms and was constant during high-frequency firing of LFHSN; transmission was progressively and reversibly abolished by replacement of Ca2+ with Mg2+. Movement of the lateral filiform hair towards the cereal tip produced a burst of spikes in LFHSN and a burst of EPSPs in GI 3. Movement of the medial filiform hair towards the base of the cercus produced a burst of spikes in the medial filiform hair sensory neurone (MFHSN) and a burst of EPSPs in GI 2. EPSPs evoked in GI 3 by LFHSN spikes were inhibited during bursts of EPSPs in GI 2 which were evoked by MFHSN spikes. LFHSN was depolarized and its spikes were reduced in amplitude during spike bursts in MFHSN. Reduction in LFHSN spike amplitude reduced GI 3 EPSPs. This phenomenon was attributed, therefore, to presynaptic inhibition. The occurrence of presynaptic inhibition was dependent upon the degree of delayed rectification exhibited by the LFHSN axon. Hyperpolarization of LFHSN increased spike height, but did not increase the amplitude of GI 3 EPSPs. The delay between the onset of MFHSN-evoked EPSPs in GI 2 and MFHSNevoked depolarizations in LFHSN suggested that MFHSN does not synapse directly onto LFHSN. Neither depolarization nor hyperpolarization of GI 2 had any effect on MFHSN-mediated presynaptic inhibition of LFHSN-GI 3 transmission, therefore it was considered unlikely that GI 2 synapses onto LFHSN. Prolonged hyperpolarization lowered the LFHSN spike threshold and temporarily abolished presynaptic inhibition. Bursts of spikes in LFHSN mediated presynaptic inhibition of MFHSN-GI2 EPSPs. Mutual presynaptic inhibition by the FHSNs may have a functional significance in sharpening the boundaries of the GIs' directional sensitivities.





2000 ◽  
Vol 203 (3) ◽  
pp. 435-445
Author(s):  
M. Wildman

The position of the coxal segment of the locust hind leg relative to the thorax is monitored by a variety of proprioceptors, including three chordotonal organs and a myochordotonal organ. The sensory neurons of two of these proprioceptors, the posterior joint chordotonal organ (pjCO) and the myochordotonal organ (MCO), have axons in the purely sensory metathoracic nerve 2C (N2C). The connections made by these afferents with metathoracic motor neurons innervating thoraco-coxal and wing muscles were investigated by electrical stimulation of N2C and by matching postsynaptic potentials in motor neurons with afferent spikes in N2C. Stretch applied to the anterior rotator muscle of the coxa (M121), with which the MCO is associated, evoked sensory spikes in N2C. Some of the MCO afferent neurons make direct excitatory chemical synaptic connections with motor neurons innervating the thoraco-coxal muscles M121, M126 and M125. Parallel polysynaptic pathways via unidentified interneurons also exist between MCO afferents and these motor neurons. Connections with the common inhibitor 1 neuron and motor neurons innervating the thoraco-coxal muscles M123/4 and wing muscles M113 and M127 are polysynaptic. Afferents of the pjCO also make polysynaptic connections with motor neurons innervating thoraco-coxal and wing muscles, but no evidence for monosynaptic pathways was found.



Development ◽  
1985 ◽  
Vol 86 (1) ◽  
pp. 227-246
Author(s):  
J. M. Blagburn ◽  
D. J. Beadle ◽  
D. B. Sattelle

The cereal afferent, giant interneurone pathway in Periplaneta americana was used as a model for synapse formation. The morphology of the two identified filiform hair sensory neurones (FHSNs) and of two giant interneurones (GI2 and GI3) was followed throughout embryogenesis by cobalt injection. The FHSN axons enter the CNS at the 45 % stage of embryogenesis, branch at 50 % and form complete arborizations by 70 %. The giant interneurones send out a primary dendrite at 45 %. Secondary branches form between 50 % and 60 % and elaboration of the branching pattern takes place until 80 % embryogenesis. At early stages the FHSN axons are within filopodial range of GI dendrites which may use these sensory processes as guidance cues. Synapse formation between the main FHSN axon shafts and GI dendrites was investigated by injection of the latter with HRP. From 55 % to 65 % the process is initiated by desmosome—like filopodial contacts, with subsequent vesicle clustering and formation of a small synaptic density. Numbers of contacts did not significantly increase after about 70 %, but the number of synapses doubled between 65 % and 75 %, with each GI process becoming postsynaptic to two FHSN synapses and the presynaptic densities lengthening to become bars. From 75 % embryogenesis to hatching there is a further small increase in synaptic bar length. In the first instar GI3 is postsynaptic to both FHSN axons, whereas GI2 forms very few synapses with the axon of the lateral FHSN (LFHSN). This imbalance of contacts is present throughout synaptogenesis, apart from some early filopodial contacts. GI3 forms synapses with the lateral side of the LFHSN axon from 60 % embryogenesis but these are totally absent at hatching. The growth of glia along this side of the axon during the last 30 % of development appears to be associated with degeneration of synapses in this region. Thus, as the dendrites of the GIs grow to form a miniature version of the adult without loss of branches, there is little evidence of an initial overproduction of FHSN—GI synapses. Similarly there is no evidence that GI2 forms ‘incorrect’ synapses with the axon of LFHSN. However, GI3 contacts are removed from an inappropriate region of a correct synaptic partner, LFHSN.





1983 ◽  
Vol 3 (4) ◽  
pp. 659-672 ◽  
Author(s):  
RK Murphey ◽  
JP Bacon ◽  
DS Sakaguchi ◽  
SE Johnson


Sign in / Sign up

Export Citation Format

Share Document