Bilateral Consequences of Chronic Unilateral Deafferentation in the Auditory System of the Cricket <i>Gryllus bimaculatus</i>

Abstract

The auditory system of the cricket has the unusual ability to respond to deafferentation by compensatory growth and synapse formation. Auditory interneurons such as ascending neuron 2 (AN-2) in the cricket Gryllus bimaculatus possess a dendritic arbor that normally grows up to, but not over, the midline of the prothoracic ganglion. After chronic deafferentation throughout larval development, however, the AN-2 dendritic arbor changes dramatically, and medial dendrites sprout across the midline where they form compensatory synapses with the auditory afferents from the contralateral ear. We quantified the extent of the effects of chronic, unilateral deafferentation by measuring several cellular parameters of 3 different neuronal components of the auditory system: the deafferented AN-2, the contralateral (or nondeafferented) AN-2 and the contralateral auditory afferents. Neuronal tracers and confocal microscopy were used to visualize neurons, and double-label experiments were performed to examine the cellular relationship between pairs of cells. Dendritic complexity was quantified using a modified Sholl analysis, and the length and volume of processes and presynaptic varicosities were assessed under control and deafferented conditions. Chronic deafferentation significantly influenced the morphology of all 3 neuronal components examined. The overall dendritic complexity of the deafferented AN-2 dendritic arbor was reduced, while both the contralateral AN-2 dendritic arbor and the remaining, intact, auditory afferents grew longer. We found no significant changes in the volume or density of varicosities after deafferentation. These complex cellular changes after deafferentation are interpreted in the light of the reported differential regulation of vesicle-associated membrane protein and semaphorin 2a.

Quantification of dendritic and axonal growth after injury to the auditory system of the adult cricket Gryllus bimaculatus

“…Deafferentation-induced elevator motor neuron sprouting in the metathoracic ganglion of locusts helps these animals recover proper wing patterns after unilateral tegula removal (Büschges et al, 1992; Wolf and Büschges, 1997). Within the cricket, deafferentation-induced compensatory dendritic responses have been demonstrated in both the terminal ganglion and the prothoracic ganglion (Murphey et al, 1975; Murphey and Levine, 1980; Hoy et al, 1985; Pallas and Hoy, 1986; Schildberger et al, 1986; Brodfuehrer and Hoy, 1988; Schmitz, 1989; Kanou et al, 2004; Horch et al, 2011; Krüger et al, 2011a,b). The deafferentation-induced compensation in the terminal ganglion consists mainly of changes in the strength of existing synapses (Murphey and Levine, 1980), though some dendritic sprouting has been noted (Murphey et al, 1975).…”

“…The deafferentation-induced compensation in the terminal ganglion consists mainly of changes in the strength of existing synapses (Murphey and Levine, 1980), though some dendritic sprouting has been noted (Murphey et al, 1975). The deafferentation-induced functional recovery in the auditory system of the cricket, on the other hand, is a result of extensive post-synaptic sprouting and reorganization as well as sprouting from intact, contralateral axons in both juveniles and adults (Schmitz, 1989; Horch et al, 2011). It is notable that functional recovery in the auditory system appears to require that axons and dendrites grow across the midline, a landmark that typically serves as an inhibitory boundary (Pallas and Hoy, 1986; Brodfuehrer and Hoy, 1988; Schmitz, 1989).…”

“…Previously, our group quantified bilateral adult auditory anatomical changes induced by chronic deafferentation throughout larval development (Horch et al, 2011). However, the quantification of the anatomical changes induced by deafferentation in the adult has been explored in only a few studies (Brodfuehrer and Hoy, 1988; Schmitz, 1989).…”

Characterization of dendritic morphology and neurotransmitter phenotype of thoracic descending propriospinal neurons after complete spinal cord transection and GDNF treatment

“…Activation of NMDA receptors stimulates dendritic outgrowth by increasing intracellular calcium (Cambray-Deakin and Burgoyne, 1992; Ciccolini et al, 2003; Hirai and Launey, 2000). Secondly, since the dPSN system is a point of convergence for various peripheral inputs, deafferentation caused by transection SCI can cause rapid dendritic atrophy of central neurons (Horch et al, 2011). Thirdly, the dendritic plasticity could reflect a compensatory response of the spinal cord to the functional deficits caused by the insult.…”

Electrophoresis of polar fluorescent tracers through the nerve sheath labels neuronal populations for anatomical and functional imaging

“…In some animals the gene-targeted expression of fluorescent proteins in specific neuronal populations has become the dominant in-vivo labelling method12. In most experimental animals however, these genetic tools are not available.…”