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. 2011 Apr 14;472(7342):213-6.
doi: 10.1038/nature09868. Epub 2011 Mar 30.

Distinct representations of olfactory information in different cortical centres

Dara L Sosulski  1 , Maria Lissitsyna Bloom, Tyler Cutforth, Richard Axel, Sandeep Robert Datta
Affiliations

Distinct representations of olfactory information in different cortical centres

Dara L Sosulski et al. Nature. .

Abstract

Sensory information is transmitted to the brain where it must be processed to translate stimulus features into appropriate behavioural output. In the olfactory system, distributed neural activity in the nose is converted into a segregated map in the olfactory bulb. Here we investigate how this ordered representation is transformed in higher olfactory centres in mice. We have developed a tracing strategy to define the neural circuits that convey information from individual glomeruli in the olfactory bulb to the piriform cortex and the cortical amygdala. The spatial order in the bulb is discarded in the piriform cortex; axons from individual glomeruli project diffusely to the piriform without apparent spatial preference. In the cortical amygdala, we observe broad patches of projections that are spatially stereotyped for individual glomeruli. These projections to the amygdala are overlapping and afford the opportunity for spatially localized integration of information from multiple glomeruli. The identification of a distributive pattern of projections to the piriform and stereotyped projections to the amygdala provides an anatomical context for the generation of learned and innate behaviours.

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Figures

Figure 1
Figure 1. Targeted electroporation of tetramethylrhodamine (TMR) dextran labels cells that innervate a single glomerulus in the olfactory bulb
A mouse olfactory bulb in which MOR 174-9 is labeled with GFP, before (a) and after (b) electroporation with TMR dextran (scale bar = 40 µM). (c) Image similar to (a) where electroporation was performed in a mouse in which synaptopHluorin is expressed in all glomeruli (OMP-IRES-spH, green); note that labeling (red) is confined to a single glomerulus (scale bar = 85 µM). (d) Control experiment in an OMP-IRES-spH mouse in which neighboring glomeruli were electroporated with TMR dextran (red, left) and fluorescein dextran (green, right, scale bar = 45 µM). (e) Labeling of mitral cells (red, green) as a result of the experiment in (d). (f) Quantification of the overlap in mitral cell labeling in experiments similar to (d) (n = 4).
Figure 2
Figure 2. Mitral/tufted cells connected to a single glomerulus exhibit distinct patterns of projections to several areas of the olfactory cortex
(a) A flattened hemi-brain preparation of the olfactory cortex with nuclei identified by counterstain (blue, NeuroTrace 435) and relevant structures outlined in white (LOT = lateral olfactory tract; AON = anterior olfactory nucleus; OT = olfactory tubercle; PIR = piriform cortex; AMG = cortical amygdala; ENT = lateral entorhinal cortex). (b) A hemi-brain from a mouse in which a single glomerulus was electroporated with TMR-dextran (red). Note the unique pattern of projection in each of the olfactory areas (scale bar = 700 µM, see also Suppl. Fig. 3).
Figure 3
Figure 3. Projections from single glomeruli to piriform cortex are disperse, homogeneous and indistinguishable
Images of axons innervating the piriform cortex (red) from mitral and tufted cells that connect to the glomerulus corresponding to MOR 1–3 (scale bar = 500 µM) (a), MOR 174-9 (b) or a random selection of glomeruli labeled with TMR-dextran (c). Correlograms plotted using the matrix of correlation coefficients generated by normalized cross-correlation of two MOR 1–3 piriforms (d), a MOR 1–3 and a MOR 174-9 piriform (e), and two piriforms in which random glomeruli were labeled (f). Cross-correlation is performed using aligned images of projection patterns as seen in (a)–(c). (g) Autocorrelograms generated using methods from (d) in which a labeled piriform is compared to itself. Note that correlograms in (g) are essentially indistinguishable from the correlograms in (d)–(f).
Figure 4
Figure 4. Projections from single glomeruli to the cortical amygdala are broad, patchy and stereotyped
Images of the cortical amygdala reveal similar projections from the mitral and tufted cells that connect to the MOR 1–3 glomerulus in two different brains (circle = approximate posterolateral cortical nucleus boundary; scale bar = 400 µM) (a), but projections that are distinct from those of mitral/tufted cells connected to the MOR 28 glomerulus (b) or six randomly selected glomeruli (c). “D” or “V” in the bottom right corner of the image indicates whether the electroporated glomerulus was located dorsally or ventrally in the bulb. (d)–(f) Counterstained images from a subregion of images in (a)–(c) displaying a closer view of projection patterns (scale bar = 400 µM). Correlograms plotted using the matrix of correlation coefficients generated by normalized cross-correlation of MOR 28 × MOR 28 projection patterns within the cortical amygdala (h), MOR 1–3 × MOR 1–3 projection patterns (i), or projection patterns from glomeruli of different types (j). (k) Autocorrelograms of the PLCo from two labeled glomeruli correlated with themselves. Note that in the en bloc preparation shown here, the lateral/medial axis (indicated by the orientation bars) is synonymous with the dorsal/ventral axis, as this region of brain is curved.
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