Multiple sources of conscious odor integration and propagation in olfactory cortex

Abstract

How do airborne plumes of molecules docking on olfactory receptors emerge as conscious odors in the brain? How are they interpreted in space, time, and biological meaning? And how do they lead to fast and adaptive decisions and actions? In general, conscious (reportable) perception supports neural adaptation to novelty, judgments of self-relevance, and voluntary decision-making. Conscious processes have a number of established properties that are markedly different from unconscious ones (Seth et al., 2005). A growing experimental literature has explored conscious perception with a wide array of recording techniques. Similarly, conscious olfaction “as such” can be studied by comparing novel vs. habituated odors, attended vs. unattended ones, and rivaling olfactory percepts, comparable to visual rivalry (Stevenson and Mahmut, 2013). State comparisons of odor processing during waking vs. sleep, general anesthesia, and impaired consciousness are also important. Neural activity underlying conscious percepts should follow the known psychophysical features of the stimulus. A specific conscious odor should correspond to a specific trajectory in the olfactory perceptual space derived from psychophysical stimulus matching and discrimination (e.g., Berglund et al., 1973; Koulakov et al., 2011). Global workspace theory (GWT) has been used as a framework for experimental studies of conscious brain processes for more than two decades, leading to a family of related models and experimental predictions. GWT begins by analyzing a reliable set of properties of conscious events (Baars, 1988, 2002). For example, while conscious perception shows limited momentary capacity, it also supports access to non-conscious functions, like memory, executive control, and automatic skills (Baars and Franklin, 2003). By comparison, unconscious stimuli do not afford such very widespread access to unconscious brain capacities. In general terms, a global workspace (GW) is a functional hub of binding and propagation in a population of loosely coupled signaling elements, such as neurons (Izhikevich, 1999). A GW is commonly compared to the stage of a theater, or a playing field in a large football arena, allowing many specialized knowledge sources to compete and cooperate to resolve focal problems. GW architectures are useful to resolve ambiguous and novel stimuli, such as words in natural language. Conscious percepts often result from a process of ambiguity reduction, and GW architectures have therefore been proposed as models of conscious perception. They are also consistent with highly interactive information flow in the cortico-thalamic (C-T) system (Baars et al., 2013). Edelman et al. (2011) suggest that GW theory is consistent with Neural Darwinism and its many ramifications. GWT predicted widespread “broadcasting” of conscious events, a prediction that is now widely accepted. In a recent study of visual rivalry in the macaque, content-specific “global broadcasting” from temporal to lateral prefrontal cortex was observed for both oscillatory population signaling and multi-unit recordings (Panagiotaropoulos et al., 2012). Similarly, long-distance cortical phase-linking is associated with the waking state but not slow-wave sleep (see Baars et al., 2013 for a review). In general, conscious sensory input has been repeatedly found to evoke more widespread, high amplitude, and phase-linked oscillations in cortex. Baars et al. (2013) have proposed that neuronal source coalitions may emerge anywhere in cortex, becoming subjectively conscious and reportable when a convergent winner-take-all source coalition comes to a momentary equilibrium, able to drive many other regions. During the waking state the visual cortex shows reentrant signaling among more than 40 visuotopical maps (Steriade, 2006). In vision the occipito-temporal cortex identifies the perceptual features that emerge in consciousness, from high-resolution visual details to lower-resolution object and event representation (IT and MTL). For the sight of a visual coffee cup or a flower garden, input convergence is believed to occur at high levels of the visual hierarchy, including object perception in area IT and event perception in MTL. However, a simple stimulus, like the sight of a single star on a dark night, might equilibrate early in the visual hierarchy, since areas V1 and LGN have the highest spatial resolution. This highly flexible version of GWT in the C-T system has been called Dynamic GWT (dGWT). Thus, visual cortex may integrate visual gestalts and broadcast them to frontoparietal, anterior temporal, and subcortical regions. In contrast, non-sensory “feelings of knowing” (FOKs), including expectations and intentions, may arise and propagate from frontal and anterior-temporal regions to caudal sites (Cole et al., 2010; Baars et al., 2013). Direct brain recordings in human patients show widespread neocortical signaling by way of cross-frequency phase-linking among cortical arrays, especially theta-gamma and alpha-gamma signaling. Single neurons have been shown to phase-adapt to dominant theta oscillations, suggesting a mechanism by which individual neurons may be recruited by population oscillations. Such spatiotemporal coding allows for an extremely rich signaling vocabulary, but specific coding schemes are just beginning to be understood (see Baars et al., 2013 for a review).