Abstract
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.
Highlights
Contrast enhancement within primary stimulus representations is a common feature of sensory systems that regulates the discrimination of similar stimuli
Each glomerulus represents a convergent population of olfactory sensory neurons expressing the same odorant receptor protein, which determines its molecular receptive range; due to this convergence, glomeruli can be treated as selective, low-noise chemosensory units [22]
The non-topographical contrast enhancement (NTCE) algorithm presented here is the basis of a novel theory of bulbar function, integrating diverse data sets gathered by several laboratories
Summary
Contrast enhancement within primary stimulus representations is a common feature of sensory systems that regulates the discrimination of similar stimuli. Primary olfactory sensory neurons (OSNs) line the nasal epithelium and respond to the presence of odors that diffuse through the nasal mucus layer and bind to olfactory receptors expressed on OSN cilia. Primary olfactory sensory neurons (OSNs) that express a given odorant receptor and exhibit a common molecular receptive range converge upon discrete glomeruli in the olfactory bulb input layer. OSN terminal arborizations form excitatory synapses with the primary dendrites of mitral (Mi), periglomerular (PG) and external tufted (ET) cells; the latter in turn activate short-axon (SA) and local PG cells. Mitral cells are the primary output neuron of the olfactory bulb, projecting via axon collaterals to several cortical and subcortical target regions [4]. Adapted from reference [2]
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