Divisive normalization in olfactory population codes

By Shawn R. Olsen, Vikas Bhandawat, Rachel I. Wilson. 2010

469 citations recorded by the source corpus.

In many regions of the visual system, the activity of a neuron is normalized by the activity of other neurons in the same region. Here we show that a similar normalization occurs during olfactory processing in the Drosophila antennal lobe. We exploit the orderly anatomy of this circuit to independently manipulate feedforward and lateral input to second-order projection neurons (PNs). Lateral inhibition increases the level of feedforward input needed to drive PNs to saturation, and this normalization scales with the total activity of the olfactory receptor neuron (ORN) population. Increasing total ORN activity also makes PN responses more transient. Strikingly, a model with just two variables (feedforward and total ORN activity) accurately predicts PN odor responses. Finally, we show that discrimination by a linear decoder is facilitated by two complementary transformations: the saturating transformation intrinsic to each processing channel boosts weak signals, while normalization helps equalize responses to different stimuli.

Subfields: Biomedical Engineering, Cellular and Molecular Neuroscience, Sensory Systems

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Citations in the corpus

Normalization as a canonical neural computation (2011, background): “The response R of an antennal lobe neuron increases with the activity I of the receptor neurons that drive i”
Normalizing the Normalizers: Comparing and Extending Network Normalization Schemes (2016, background): “weights. Previous theoretical studies have outlined several potential computational roles for divisive normalization such as sensitivity maximization (Carandini & Heeger, 2012), invariant coding (Olsen et al., 2010), density modelling (Balle et al., 2016), image compression (Malo et al., 2006), ”
Neuronal mechanisms underlying innate and learned olfactory processing in Drosophila. (2019, background): “This ‘input gain control’ normalizes responses by total ORN activity, 71 decreases correlations between odor response profiles of different PNs [12], and improves 72 odor discrimination by a perceptron modelling neurons post-synaptic to PNs [14].”
A Normalization Model of Multisensory Integration (2011, unknown): “The apparent ubiquity of divisive normalization in neural circuits 36, 45 makes normalization operating at the level of multisensory integration an attractive general model to account for cross-modal interactions.”
Neurogenesis Drives Stimulus Decorrelation in a Model of the Olfactory Bulb (2012, background): “ cells, and external tufted cells in the glomerular layer of the olfactory bulb [69]. Divisive normalization has been observed in the antennal lobe, which is the insect analogue of the olfactory bulb [70]. Implemented in simulations by global lateral inhibition, it was found to reduce the correlatio”
The neuroscience of learning: beyond the Hebbian synapse. (2013, background): “…is a form of lateral inhibition in which the response of one neuron in a class of neurons (e.g., the simple cells in V1) is suppressed in proportion to the inverse of the sum of the responses of the other neurons in its class (see, e.g., Heeger 1992, Olsen et al. 2010, Simoncelli & Heeger 1998).”
Cellular-resolution population imaging reveals robust sparse coding in the Drosophila Mushroom Body (2011, background): “This subadditivity is consistent with observations made in the antennal lobe (Silbering and Galizia, 2007; Olsen et al., 2010) and olfactory bulb (Meredith, 1986; Tabor et al., 2004) and is a well known olfactory phenomenon termed mixture suppression (Moskowitz and Barbe, 1977).”
Odor Discrimination in Drosophila: From Neural Population Codes to Behavior (2013, methodology): “…synaptic relays, the glomeruli of the antennal lobe, to discrete classes of excitatory projection neurons (ePNs) (Jefferis et al., 2001; Stocker et al., 1990). ePN responses are saturating functions of input from cognate ORNs that scale inversely with total ORN activity (Olsen et al., 2010).”
Parvalbumin-expressing interneurons linearly control olfactory bulb output (2013, unknown): “In the Drosophila antennal lobe, an insect analog of the olfactory bulb, the strength of inhibition is proportional to the total amount of excitatory sensory input (divisive normalization) (Olsen et al., 2010; Olsen and Wilson, 2008).”
RULES OF COMPETITIVE STIMULUS SELECTION IN A CHOLINERGIC ISTHMIC NUCLEUS OF THE OWL MIDBRAIN (2011, unknown): “B, Input division, The SiRP was shifted rightward by 3°/s (Olsen et al., 2010).”
Activity of Defined Mushroom Body Output Neurons Underlies Learned Olfactory Behavior in Drosophila (2015, background): “…the same glomerulus in each antennal lobe (Vos- shall, 2000; Gao et al., 2000; Couto et al., 2005; Fishilevich and Vosshall, 2005), where their activity is relayed to excitatory and inhibitory projection neurons (Olsen et al., 2010; Kazama and Wilson, 2008; Parnas et al., 2013; Liang et al., 2013).”