RESUBMISSION: Neural processing underlying auditory pattern recognition in an insect brain

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Neuroscience aims at understanding how sensory pathways are organised, how stimuli are processed and how features are extracted to elicit an appropriate motor response. Especially in intraspecific communication the recognition of specific stimulus features plays an important role as species-specific olfactory, visual and/or acoustic signals are employed for mate attraction and rivalry behaviour. As sounds are always transient, signalling by repetitive patterns of pulses is central to acoustic communication in many vertebrates and invertebrates. Especially frogs and insects like bush-crickets and crickets use simple sound pulses generated with species-specific temporal patterns for communication. In the auditory pathway of the receiver, these signals require neural filter mechanisms that respond to the temporal structure of sound patterns. Considerable progress has been made in frogs in describing brain neurons with selective tuning to pulse patterns. However, there is still a very limited understanding of neurons underlying temporal processing of sound patterns in crickets although since decades they are a model system for insect hearing. Female crickets are attracted to the species-specific pattern of male calling song. In behavioural experiments we demonstrated the tuning of their phonotactic behaviour to changes in pulse interval, pulse duration and chirp interval. For example their phonotactic behaviour is tuned to the pulse pattern of the male song as pulses with shorter or longer periods are not attractive. We now aim to understand at the level of identified neurons the filter mechanisms in the brain that allow the recognition of the species-specific song pattern.The ascending auditory interneuron that forwards the pulse pattern of the calling song from the first thoracic ganglion to the brain exhibits no filter properties. Hypothesis for temporal filtering in the brain have been put forward, however, the actual neural mechanisms have not been revealed. In preliminary experiments we identified local brain neurons which form a ring-like auditory neuropil in the protocerebrum matching the axonal arborisations of the ascending interneuron. Some of these neurons showed a selective response to the pulse interval of the calling song and received inhibitory and excitatory synaptic inputs. In other systems the interaction between inhibition and excitation is crucial for selectivity to pulse patterns. Using the same acoustic paradigms as in the behavioural studies we will analyse the activity of auditory brain neurons. We will focus on four questions: 1). Which brain neurons are involved in temporal filtering of acoustic pulse patterns?2). What are the neural mechanisms underlying temporal filtering? 3). What is the structural and functional organisation of the auditory neuropil?4). Which projection neurons connect the auditory neuropil to other brain regions?The project will be based on our experience of recording intracellularly the activity of auditory brain neurons with sharp microelectrodes. The neural responses will be compared with our behavioural data and quantitative analysis will reveal to what degree the activity of single neurons mirrors the behavioural tuning. The pattern of inhibitory and excitatory synaptic activity will provide crucial information on how temporal filtering is achieved within the auditory network. We will manipulate the membrane potential of neurons by intracellular current injection to analyse the nature of the neural filter mechanisms in detail. Finally we will use confocal microscopy to reveal the structural details of these neurons in the brain and we will identify neurons which link the auditory neuropil to other areas of the brain. The analysis of the pattern recognition network in crickets will provide insight to principle mechanisms of temporal filtering at the level of identified neurons and can be a model for temporal selectivity in other systems.