Dynamic dendritic compartmentalization underlies stimulus-specific adaptation in an insect neuron

Abstract

Prešern J, Triblehorn JD, Schul J. Dynamic dendritic compartmentalization underlies stimulus-specific adaptation in an insect neuron. J Neurophysiol 113: 3787-3797, 2015. First published April 15, 2015 doi:10.1152/jn.00945.2014.-In many neural systems, repeated stimulation leads to stimulus-specific adaptation (SSA), with responses to repeated signals being reduced while responses to novel stimuli remain unaffected. The underlying mechanisms of SSA remain mostly hypothetical. One hypothesis is that dendritic processes generate SSA. Evidence for such a mechanism was recently described in an insect auditory interneuron (TN-1 in Neoconocephalus triops). Afferents, tuned to different frequencies, connect with different parts of the TN-1 dendrite. The specific adaptation of these inputs relies on calcium and sodium accumulation within the dendrite, with calcium having a transient and sodium a tonic effect. Using imaging techniques, we tested here whether the accumulation of these ions remained limited to the stimulated parts of the dendrite. Stimulation with a fast pulse rate, which results in strong adaptation, elicited a transient dendritic calcium signal. In contrast, the sodium signal was tonic, remaining high during the fast pulse rate stimulus. These time courses followed the predictions from the previous pharmacological experiments. The peak positions of the calcium and sodium signals differed with the carrier frequency of the stimulus; at 15 kHz, peak locations were significantly more rostral than at 40 kHz. This matched the predictions made from neuroanatomical data. Our findings confirm that excitatory postsynaptic potentials rather than spiking cause the increase of dendritic calcium and sodium concentrations and that these increases remain limited to the stimulated parts of the dendrite. This supports the hypothesis of "dynamic dendritic compartmentalization" underlying SSA in this auditory interneuron.

Auditory DUM neurons in a bush‐cricket: A filter bank for carrier frequency

“…The structure and response properties of prothoracic auditory interneurons are well studied (Atkins & Pollack, ; Kostarakos & Römer, ; Rheinlaender, ; Stumpner & Molina, ; Triblehorn & Schul, ), but little is known about the prothoracic auditory network and its functional design (Molina & Stumpner, ; Pollack & Imaizumi, ; Römer et al, ; Triblehorn & Schul, ). Experimental evidence indicates that local prothoracic neurons contribute to the processing of sound direction, carrier frequency, and temporal patterns in crickets (Faulkes & Pollack, ; Hardt & Watson, ; Selverston et al, ) and bush‐crickets (Prešern et al, ; Rheinlaender, ; Römer, ; Römer et al, ; Schul, ; Stumpner, ; Stumpner & Molina, ). However, besides the prominent omega neuron (ON1, Popov et al, ; Zhantiev & Korsunovskaya, ), only few local sound activated neurons in Ensifera have been studied (Stiedl et al, ; Stritih & Stumpner, ; Zhantiev & Korsunovskaya, ).…”

Multivariate female preference tests reveal latent perceptual biases

“…Potentially, the pulse rates of these species are sufficiently low as to escape the 40 -60 ms NA time constants described in the auditory pathway of crickets [43]. Interestingly, in the katydid Neoconocephalus triops, Prešern et al [44] have recently shown strong NA at the neuronal level to fast (140 p s 21 ) sound pulses but a lack of NA to slow (7 p s 21 ) sound pulses. It is also possible that the slow pulse rate does not play an important role, and these species simply show reduced or absent NA for other unknown reasons.…”

Insect Hearing

“…When the frequency spectra do differ, the strength of synaptic input from afferents may be much stronger for ultrasound than for sonic conspecifi c signals . Furthermore, local processing within a neuron's extended dendrites may allow segregation of signals differing in spectral content and temporal pattern Prešern et al 2015 ), implementing a form of auditory scene analysis or stream segregation analogous to mechanisms described for vertebrates (Moss and Surlykke 2010 ).…”