Figure 1.

(a) Circuit diagram of the mammalian olfactory bulb. The axons of olfactory sensory neurons expressing the same odorant receptor type converge together as they cross the cribriform plate and arborize together to form glomeruli (shaded ovals) across the surface of the olfactory bulb. Several classes of olfactory bulb neuron innervate each glomerulus, including both principal neurons and intrinsic interneurons. Glomerular interneuron classes are heterogeneous, including olfactory nerve-driven periglomerular cells (PGo), external tufted cell-driven periglomerular cells (PGe), and multiple subtypes of external tufted cells (ET). Superficial short-axon cells (sSA) are not associated with specific glomeruli but project broadly and laterally within the deep glomerular layer, interacting with glomerular interneurons. Principal neurons include mitral cells (Mi), which interact via reciprocal connections in the external plexiform layer (EPL) with the dendrites of inhibitory granule cells (Gr), thereby receiving recurrent and lateral inhibition. Middle/deep tufted cells (not depicted) constitute another, less understood class of olfactory bulb principal neurons noted for their relative lack of an inhibitory surround. Both of these principal neuron types project divergently to several regions of the brain, though the projection profiles of the two classes differ [71, 90]. A sparse, heterogeneous population of inhibitory interneurons known collectively as deep short-axon cells [91] also is not depicted. OE, olfactory epithelium (in the nasal cavity); GL, glomerular layer; EPL; external plexiform layer; MCL, mitral cell layer; IPL, internal plexiform layer; GCL, granule cell layer. Filled triangles denote excitatory (glutamatergic) synapses; open circles denote inhibitory (GABAergic) synapses. (b) Schematic depiction of decorrelation between two overlapping representations (α and β), depicted in one dimension (left panel). Canonical “Mexican-hat” decorrelation (upper right panel) generates an explicit inhibitory surround in which the edges of the representation are inhibited below baseline, yielding a sharp reduction in overlap among similar representations. This computation is performed by lateral inhibition in the retina and inferior colliculus, and by the nontopographical model of olfactory receptive field decorrelation. A lesser degree of decorrelation can also be obtained by broad, nonspecific inhibition, including lateral inhibition with an unstructured surround [45, 46] (lower right panel), although this imposes a general reduction in activity across the entire representation. This operation is the general result of lateral inhibitory mechanisms as studied to date in the olfactory bulb. While both computations can effect a measurable decorrelation, the two transformations differ substantially. (c) Replication of experimental data from [23] by the nontopographical model [26] demonstrating Mexican-hat decorrelation in mitral cells among the responses to similar odorants (3-carbon through 11-carbon aliphatic aldehydes). Periodic bursts of spikes reflect background activity evoked by the respiration cycle; a 2 second odorant stimulus was presented during the third inhalation (black bar; green shading). The odorant hexanal ((6)CHO) is near the center of this mitral cell's receptive field and evokes the strongest activation; pentanal and heptanal also excite the cell, whereas butanal ((4)CHO) and octanal ((5)CHO) are within its inhibitory surround, and hence evoke a net inhibition. The mitral cell is unresponsive to the other four odorants. The right panel illustrates how the Mexican-hat function maps onto the trajectory through odor similarity space defined by the homologous odor series. Plus sign connotes excitation; minus sign connotes inhibition. Figure adapted from ref. [26].