Cortical representations of olfactory input by trans-synaptic tracing

• Published in: Nature (London) Vol. 472; no. 7342; pp. 191 - 196
• Main Authors: Miyamichi, Kazunari, Amat, Fernando, Moussavi, Farshid, Wang, Chen, Wickersham, Ian, Wall, Nicholas R., Taniguchi, Hiroki, Tasic, Bosiljka, Huang, Z. Josh, He, Zhigang, Callaway, Edward M., Horowitz, Mark A., Luo, Liqun
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 14.04.2011; Nature Publishing Group
• Subjects: 631/1647/245/2227; 631/378/2571/1696; 631/378/2624; 631/378/548; Amygdala - anatomy & histology; Amygdala - cytology; Amygdala - physiology; Animals; Axons - physiology; Behavior; Bias; Biological and medical sciences; Brain; Brain Mapping; Experiments; Fundamental and applied biological sciences. Psychology; Genetic aspects; Genetic engineering; Genetics; HEK293 Cells; Humanities and Social Sciences; Humans; Methods; Mice; Mice, Transgenic; multidisciplinary; Neural transmission; Neuroanatomical Tract-Tracing Techniques; Neurons; Odorants - analysis; Olfactory Bulb - anatomy & histology; Olfactory Bulb - cytology; Olfactory Bulb - physiology; Olfactory cortex; Olfactory Pathways - anatomy & histology; Olfactory Pathways - cytology; Olfactory Pathways - physiology; Olfactory Perception - genetics; Olfactory Perception - physiology; Olfactory Receptor Neurons - cytology; Olfactory Receptor Neurons - physiology; Olfactory system and olfaction. Gustatory system and gustation; Physiological aspects; Rabies; Rabies virus - physiology; Science; Science (multidisciplinary); Somesthesis and somesthetic pathways (proprioception, exteroception, nociception); interoception; electrolocation. Sensory receptors; Synapses - genetics; Synapses - metabolism; Vertebrates: nervous system and sense organs; Viral infections; United States; Olfactory cortex; Amygdala; Rodentia; Central nervous system; Projection; Nervous system; Basal ganglion; Olfactory receptor; Sensory receptor; Encephalon; Associative memory; Vertebrata; Mammalia; Olfactory pathway; Neuron; Mouse; Piriform cortex; Preference; Animal; Olfactory bulb; Olfactory glomerulus; Biological receptor
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature09714

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. Scent tracking In the mouse, glomeruli in the olfactory bulb receive projections from single classes of olfactory neurons, thereby forming an odour map. Information from the glomeruli is then relayed to the cortex but the projection patterns from individual glomeruli are not known. Three papers now examine the details of this projection. Luo and colleagues use a combination of genetics and retrograde mono-trans-synaptic rabies virus labelling. They trace the presynaptic connections of individual cortical neurons and find no evidence of connections supporting a stereotyped odour map in the cortex, but see systematic topographical differences in amygdala connectivity. The lack of stereotypical cortical projection is corroborated, both at the level of bulk axonal patterning and in projections of individually labelled neurons, by two papers — one from the Axel laboratory, and one from the Baldwin laboratory — that examine the anterograde projections from individual glomeruli. Together, these findings provide anatomical evidence for combinatorial processing of information from diverse glomeruli by cortical neurons and may also reflect different functions of various areas in mediating innate or learned odour preferences.