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In the mouse, each class of olfactory receptor neurons expressing a given odorant receptor has convergent axonal projections to two specific glomeruli in the olfactory bulb, thereby creating an odour map. However, it is unclear how this map is represented in the olfactory cortex. Here we combine rabies-virus-dependent retrograde mono-trans-synaptic labelling with genetics to control the location, number and type of 'starter' cortical neurons, from which we trace their presynaptic neurons. We find that individual cortical neurons receive input from multiple mitral cells representing broadly distributed glomeruli. Different cortical areas represent the olfactory bulb input differently. For example, the cortical amygdala preferentially receives dorsal olfactory bulb input, whereas the piriform cortex samples the whole olfactory bulb without obvious bias. These differences probably reflect different functions of these cortical areas in mediating innate odour preference or associative memory. The trans-synaptic labelling method described here should be widely applicable to mapping connections throughout the mouse nervous system.
The functions of mammalian brains are based on the activity patterns of large numbers of interconnected neurons that form information processing circuits. Neural circuits consist of local connections- where pre- and postsynaptic partners reside within the same brain area-and long-distance connections, which link different areas. Local connections can be predicted by axon and dendrite reconstructions1, and confirmed by physiological recording and stimulation methods2. Long-distance connections are more difficult to map, as commonly used methods can only trace bulk projections with a coarse resolution. Most methods cannot distinguish axons in passing from those that form synapses, or pinpoint the neuronal types to which connections are made1,2. Trans-synaptic tracers can potentially overcome these limitations2. Here we combine a retrograde rabies-virusdependent mono-trans-synaptic labelling technique3 with genetic control of the location, number and cell type of 'starter' neurons to trace their presynaptic partners. We systematically mapped longdistance connections between the first olfactory processing centre, the olfactory bulb, and its postsynaptic targets in the olfactory cortex including the anterior olfactory nucleus (AON), piriform cortex and amygdala (Supplementary Fig. 1).
Genetic control of trans-synaptic tracing
Rabies virus can cross synapses from postsynaptic to presynaptic neurons with high specificity4, without notable defects in the morphology or physiology of infected neurons for extended periods of time3,5. Recent genetic modifications of rabies virus have permitted mono-trans-synaptic labelling3. Specifically,...