Olfactory Coding with Patterns of Response Latencies

Abstract

The encoding of odors by spatiotemporal patterns of mitral/tufted (M/T) cells in the vertebrate olfactory bulb has been discussed controversially. Motivated by temporal constraints from behavioral studies, we investigated the information contained in odor-evoked first-spike latencies. Using simultaneous recordings of dozens of M/T cells with a high temporal resolution and quantitative ensemble correlation techniques, we show that latency patterns, and in particular latency rank patterns, are highly odor specific and reproducible. They reliably predict the odor identity as well as the odor concentration on a single-trial basis and on short timescales-in fact, more reliably than patterns of firing rates. Furthermore, we show that latency ranks exhibit a better reproducibility at the level of M/T cells than in olfactory receptor neurons. Our results suggest that the latency patterns of M/T cells contain all the information higher brain centers need to identify odors and their concentrations.

Complementary codes for odor identity and intensity in olfactory cortex

“…Our results are partially consistent with a prevailing model, initially proposed by Hopfield, for how odor representations are transformed and encoded in olfactory bulb, and could be decoded in piriform cortex (Hopfield, 1995; Schaefer and Margrie, 2007; Junek et al, 2010; Schaefer and Margrie, 2012; Uchida et al, 2014; Wilson et al, 2015). This model gives rise to several predictions: (1) The earliest-activated mitral cells will largely define the odor representation, and thus the ensemble of activated cortical cells, with later responses suppressed or ‘discriminated against’ (Hopfield, 1995); (2) Odor identity can be extracted from the sequence of the earliest-activated mitral cell responses and transformed into a representation that is robust to changes in concentration; (3) Spike time information should not inform representations of odor identity in cortex; (4) Odor intensity can be extracted from the latency to spike of the earliest-activated mitral cells.…”

Distributed organization of a brain microcircuit analyzed by three-dimensional modeling: the olfactory bulb

“…These characteristics were in accord with experimental findings (Chen and Shepherd, 1997; Hovis et al, 2010). Two other important properties for odor processing are the latency of the first spike in response to odor input (Junek et al, 2010), and the firing rate (Shusterman et al, 2011; Smear et al, 2011). This is shown for the model of a typical cell in Figure 5A bottom, for a single simulated sniff as a function of the odor concentration, as measured by the total peak synaptic conductance activated on the mitral cell tuft.…”

Paying attention to smell: cholinergic signaling in the olfactory bulb

“…Odor-evoked responses are not encoded in simple changes in firing frequencies; instead, the OB adopts various sophisticated mechanisms, involving the activity of MCs, to detect and encode odors. For example, upon odor onset, the latency of the first MC spike in response to the odor (Margrie and Schaefer, 2003; Junek et al, 2010), reduction in MC firing frequency (Rinberg and Gelperin, 2006; Rinberg et al, 2006; Davison and Katz, 2007), alterations in the relative temporal phase of individual spikes (Dhawale et al, 2010), relative timing of MC spikes (Haddad et al, 2013), and fine-scale changes in temporal spike patterns (Friedrich and Laurent, 2001; Cury and Uchida, 2010) are all thought to play important roles in odor coding. Each of these mechanisms is a potential target for modulation, thus leading to a multifold increase in the computational power of the OB.…”