Computational Modeling Suggests That Response Properties Rather Than Spatial Position Determine Connectivity Between Olfactory Glomeruli

Abstract

Linster, Christiane, Silke Sachse, and C. Giovanni Galizia. Computational modeling suggests that response properties rather than spatial position determine connectivity between olfactory glomeruli. J Neurophysiol 93: 3410 -3417, 2005. First published January 26, 2005 doi:10.1152/jn.01285.2004. Olfactory responses require the representation of high-dimensional olfactory stimuli within the constraints of two-dimensional neural networks. We used a computational model of the honeybee antennal lobe to test how inhibitory interactions in the antennal lobe should be organized to best reproduce the experimentally measured input-output function in this structure. Our simulations show that a functionally organized inhibitory network, as opposed to an anatomically or all-to-all organized inhibitory network, best reproduces the input-output function of the antennal lobe observed with calcium imaging. In this network, inhibition between each pair of glomeruli was proportional to the similarity of their odor-response profiles. We conclude that contrast enhancement between odorants in the honeybee antennal lobe is best achieved when interglomerular inhibition is organized based on glomerular odor response profiles rather than on anatomical neighborhood relations. I N T R O D U C T I O NOlfactory representations are intrinsically high dimensional yet must be represented within morphologically two-dimensional neural networks. A great deal of research in olfaction has focused on the representation of olfactory information within the first processing stage, the olfactory bulb (OB) or antennal lobe (AL) glomeruli, particularly with respect to how chemical stimuli are mapped onto olfactory glomeruli and how this mapping may relate to their perceptual qualities (Galizia and Menzel 2001;Linster et al. 2001;Xu et al. 2000). While a number of studies have illustrated the importance of inhibitory networks within the OB or AL for the shaping and processing of olfactory information (Stopfer et al. 1997;Urban 2002;Yokoi et al. 1995), it is not clear how exactly these inhibitory networks are organized to provide filtering and contrast enhancement capabilities. It is generally believed that odors are represented as combinatorial activity patterns across olfactory glomeruli; odor-specific spatiotemporal activity patterns in olfactory glomeruli have been shown in vertebrates (Meister and Bonhoeffer 2001;Rubin and Katz 1999;Wachowiak et al. 2000Wachowiak et al. , 2002 and invertebrates (Christensen et al. 2000; Faber et al. 1999; Galizia and Menzel 2000; Hansson et al. 2003; Joerges et al. 1997;Sachse et al. 1999). It has been suggested that the broadly distributed activation patterns observed at the glomerular layer can be modulated by the OB/AL network in such a way as to ensure specific discrimination between chemically similar odorants (Duchamp-Viret and Duchamp 1993; Linster and Gervais 1996; Linster and Hasselmo 1997; Meredith 1986; Sachse and Galizia 2002; Urban 2002). Specifically, using calcium imaging in the AL of honeybees, we hav...

Chemosensory Selectivity of Output Neurons Innervating an Identified, Sexually Isomorphic Olfactory Glomerulus

“…8). This agrees with results from other authors (Sachse and Galizia, 2002;Linster et al, 2005), who reported that response properties rather than spatial position determine interglomerular interactions.…”

Mind the Gap: Olfactory Trace Conditioning in Honeybees

“…Thus, generalization can be used as a tool to measure the perceived quality of a CS in relation to other test odors. If trace and delay conditioning engage different brain areas, as is the case in mammals (Woodruff-Pak and Disterhoft, 2008), one would expect differences in the perceived odor quality between trace and delay conditioning, because neural odor representations change over time (Galán et al, 2004) and along different processing levels of the olfactory pathway (Linster et al, 2005;Szyszka et al, 2005). We therefore asked whether the perceived odor quality differs between trace memory and delay conditioning (Fig.…”

Olfactory Information Processing in theDrosophilaAntennal Lobe: Anything Goes?

“…Several studies have proposed processing mechanisms that appear to contradict each other: while it has been shown that interglomerular connectivity in the antennal lobe narrows odor response profiles in honeybees (Sachse and Galizia, 2003;Linster et al, 2005), reports in Drosophila support either a neutral effect of the antennal lobe network in the propagation of olfactory information (Ng et al, 2002;Wang et al, 2003) or a broadening of the response profiles at the PN level (Wilson et al, 2004).…”