Auditory brain neurons underlying temporal pattern recognition and phonotaxis
Females crickets are attracted to male calling song and walk towards singing males. Their phonotactic behaviour shows clear band-pass tuning as the response decays when pulse intervals are lower or higher as in the normal calling song. Temporal filtering occurs in the brain as identified ascending interneurons copy and forward the pulse pattern to the brain without any preference. Selectivity for the species-specific song pattern might be due to sequential low-pass and high-pass filtering,however, the actual neural mechanisms underlying auditory pattern recognition and phonotaxis is still not resolved. We started to analyse the question of pattern recognition by recording auditory brain neurons in walking crickets.
We focus on following crucial questions:
- How is the local network of auditory brain neurons organized?
- Which neural mechanisms underlie pattern recognition?
- Which descending interneurons controlling phonotactic walking are driven by the network of auditory brain neurons?
Using sharp microelectrodes we record the activity of auditory brain neurons. Females are walking on a high-resolution trackball that precisely monitors the forward and lateral movement components of their walking behaviour. While sound patterns are presented by a left and right speaker, we test if brain neurons have an impact on auditory steering by modulating their spike activity with intracellular current injection (Fig. 1 and 2). Finally brain neurons are labeled with a fluorescent marker to reveal their projection areas and their structure is reconstructed using confocal microscopy.
Our preliminary results demonstrate that in each half of the brain at least three types of local auditory brain neurons form a dense auditory neuropil in the anterior protocerebrum. This neuropil is organized along the ring-like axonal arborisations of the ascending interneuron AN1. Local neurons intrinsic to the neuropil are depolarised by sound pulses and their spike activity precisely copies the pulse pattern as mediated by the ascending interneuron AN1.
Local neurons with axons connecting both auditory neuropils receive a combination of inhibitory and excitatory inputs, with inhibition dominating the response towards the first pulse of a chirp. The spiking response of these neurons depends on the pulse interval of the test pattern and is best, when the pulse interval corresponds to the species-specific pattern. These neurons therefore show band-pass properties indicating that pattern recognition may occur at a very early stage of auditory processing in the brain due a mixed processing of inhibitory and excitatory synaptic inputs.
We now focus on identifying brain neurons that project from the auditory neuropil towards descending interneurons involved in controlling walking and phonotaxis. Preliminary data indicate that the lateral accessory lobes may be an important interface to forward auditory activity to descending interneurons controlling phonotaxis.
Publications from my PhD:
- Kostarakos K., Rheinländer J. and Römer H. (2007) Spatial orientation in the bushcricket Leptophyes punctatissima (Phaneropterinae; Orthoptera): III. Peripheral directionality and central nervous processing of spatial cues. J Comp Physiol A. 193:1115–1123.
- Kostarakos K., Hartbauer M. and Römer H. (2008) Matched filters, mate choice and the evolution of sexually selected traits. PloS ONE 3(8): e3005.
- Kostarakos K., Hennig M. and Römer H. (2009) Two matched filters and the evolution of mating signals in four species of cricket. Frontiers in Zoology 6:22.
- Kostarakos K. and Römer H. (2010) Sound transmission and directional hearing in field crickets: neurophysiological studies outdoors. J Comp Physiol A. 196:669-681
Group Members
Dr Berthold Hedwig (Group Leader)
bh202@cam.ac.uk
Dr Fabienne Dupuy
Research: Auditory motor interface
fyd20@cam.ac.uk
Dr Kostas Kostarakos
Research: Auditory brain neurons
kk437@cam.ac.uk
Dr Stefan Schoeneich
Research:Song pattern generation
ss817@cam.ac.uk
Kelly Seagraves
Research: Directional sensitivity
ks584@cam.ac.uk
Part II Zoology Project Students
Tanya Gunnarsdottir
Gemma Longson