Non-topographical contrast enhancement in the olfactory bulb

By Thomas A. Cleland, Praveen Sethupathy. 2006

191 citations recorded by the source corpus.

BackgroundContrast enhancement within primary stimulus representations is a common feature of sensory systems that regulates the discrimination of similar stimuli. Whereas most sensory stimulus features can be mapped onto one or two dimensions of quality or location (e.g., frequency or retinotopy), the analogous similarities among odor stimuli are distributed high-dimensionally, necessarily yielding a chemotopically fragmented map upon the surface of the olfactory bulb. While olfactory contrast enhancement has been attributed to decremental lateral inhibitory processes among olfactory bulb projection neurons modeled after those in the retina, the two-dimensional topology of this mechanism is intrinsically incapable of mediating effective contrast enhancement on such fragmented maps. Consequently, current theories are unable to explain the existence of olfactory contrast enhancement.ResultsWe describe a novel neural circuit mechanism, non-topographical contrast enhancement (NTCE), which enables contrast enhancement among high-dimensional odor representations exhibiting unpredictable patterns of similarity. The NTCE algorithm relies solely on local intraglomerular computations and broad feedback inhibition, and is consistent with known properties of the olfactory bulb input layer. Unlike mechanisms based upon lateral projections, NTCE does not require a built-in foreknowledge of the similarities in molecular receptive ranges expressed by different olfactory bulb glomeruli, and is independent of the physical location of glomeruli within the olfactory bulb.ConclusionNon-topographical contrast enhancement demonstrates how intrinsically high-dimensional sensory data can be represented and processed within a physically two-dimensional neural cortex while retaining the capacity to represent stimulus similarity. In a biophysically constrained computational model of the olfactory bulb, NTCE successfully mediates contrast enhancement among odorant representations in the natural, high-dimensional similarity space defined by the olfactory receptor complement and underlies the concentration-independence of odor quality representations.

Subfields: Cellular and Molecular Neuroscience, Insect Science, Sensory Systems

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Citations in the corpus

Re-evaluating circuit mechanisms underlying pattern separation (2019, positive): “This overall arrangement of inhibition is consistent with the theory of non-topographical contrast enhancement (Cleland and Sethupathy, 2006), which implements a weak version of a winnertake-all algorithm that is well suited for high dimensional representations that cannot be represented in a smooth”
Timescale-dependent shaping of correlation by olfactory bulb lateral inhibition (2011, background): “Unlike purely center-surround lateral inhibitory circuits (such as the retina) (55), olfactory bulb lateral inhibition is less topographically confined (11, 56, 57) and mitral cells can laterally influence distant cells (37, 58–60).”
Mechanisms of pattern decorrelation by recurrent neuronal circuits (2010, background): “In principle, pattern decorrelation could also be achieved by other nontopographic mechanism”
Inhibitory circuits of the mammalian main olfactory bulb. (2017, background): “First, as discussed elsewhere (Cleland and Sethupathy 2006), GABAAR antagonists are not specific to GCs.”
Neurogenesis Drives Stimulus Decorrelation in a Model of the Olfactory Bulb (2012, background): “If neurogenesis were to affect only interneurons that provide non-topographic inhibition and no lateral inhibition [4] both enrichment protocols would be expected to lead to the same level of decorrelation.”
Divisive normalization in olfactory population codes (2010, result): “…our results is a recent theoretical study pointing out that global lateral inhibition should decorrelate the odor selectivity of different glomeruli (Cleland and Sethupathy, 2006), although that study postulated a different type of intraglomerular transformation than the function we describe here.”
Independent control of gamma and theta activity by distinct interneuron networks in the olfactory bulb (2014, unknown): “Thus, in contrast to common belief 19-21 , it is the glomerular circuitry, likely via a feedforward inhibitory pathway, rather than the lateral inhibition by GCs, that underlies evoked inhibition on slow timescales and potentially contrast enhancement 22 .”