One respiratory cycle as a minimum time unit for making behavioral decisions in the mammalian olfactory system

Abstract

Voluntary behaviors such as sniffing, moving, and eating require decision-making accompanied by intentional respiration. Based on the study of respiration-coherent activity of rodent olfactory networks, we infer that during the inhalation phase of respiration, olfactory cortical areas process environmental odor information and transmit it to the higher multisensory cognitive areas via feedforward pathways to comprehensively evaluate the surrounding situation. We also infer that during the exhalation phase, the higher multisensory areas generate cognitive-signals and transmit them not only to the behavioral output system but also back to the olfactory cortical areas. We presume that the cortical mechanism couples the intentional respiration with the voluntary behaviors. Thus, in one respiratory cycle, the mammalian brain may transmit and process sensory information to cognize and evaluate the multisensory image of the external world, leading to one behavioral decision and one emotional expression. In this perspective article, we propose that one respiratory cycle provides a minimum time unit for decision making during wakefulness.

Keywords: behavioral decisions; inhalation and exhalation; olfactory system; one respiratory cycle-one decision making; sensory inputs; voluntary behaviors.

Figure 1

(A) A schematic diagram of the central olfactory areas. The presumed feedforward transmission of external odor information (during inhalation) and possible top–down transmission of cognitive signals (during exhalation) are shown. Orange arrows show the feedforward transmission of external odor signals from the lower cortical area to the superficial layer (yellow) of the higher cortical area during inhalation. Blue arrows are for the top–down transmission of cognitive signals from the higher cortical area to the deep layers (blue) of the lower cortical area during exhalation. Olfactory cortical areas (solid gray boxes) include the olfactory bulb (OB), anterior olfactory nucleus pars externa (AONe), anterior olfactory nucleus pars lateralis [AON(l)], anterior piriform cortex (APC), posterior piriform cortex (PPC), lateral entorhinal cortex (LEC), and cortical nucleus of amygdala (CoA). Higher-order multisensory cognitive areas (broken line boxes) include the orbitofrontal cortex (OFC), ventral agranular insular cortex (AIV), medial prefrontal cortex (mPFC), and basal amygdaloid nucleus (BA). Abbreviations for the layers: GlL, glomerular layer; EPL, external plexiform layer; MCL, mitral cell layer; GCL, granule cell layer; Ia, layer Ia; Ib, layer Ib; II, layer II; III, layer III; SL, superficial layer; and DL; deep layer. Abbreviations for the cells: eTC, external tufted cell; mTC, middle tufted cell; MC, mitral cell; Py, pyramidal cell; Py*, pyramidal cell of the AON(l) that projects apical dendrites to the layer Ia of the AONe; SeL, semilunar cell; SPy, superficial pyramidal cell; and DPy, deep pyramidal cell. (B) Depth profiles and current-source-density analysis of local field potentials recorded at intervals of 100 μm in depth in the AON(l) and APC of the awake resting rats. The raw local field potential was band-pass filtered (0.5–3 Hz) and current-source-density was calculated. Warm colors indicate the current-sink, while cold colors show the current-source. Respiration was monitored by a thermocouple placed at the nostril (RESP, shown in the bottom trace). The inhalation phase (Inh) is in orange, while exhalation phase (Exh) is in blue. Only slow-wave current-sinks are shown, but not the β-and γ-range fast oscillatory current-sinks, because of the band-pass filtering. Downward arrowheads indicate slow-wave current-sinks in the superficial layer while upward arrowheads indicate slow-wave current-sinks in the deep layer. The figures are modified from Narikiyo et al. (2018).

Figure 2

(A) A model of neural networks that may mediate behavioral decision-making. Information flow for external odors (broken arrows) and neural networks that couple the intentional respiration with the voluntary behaviors (solid arrows) are shown. Abbreviations: BF, basal forebrain; BötC, Bötzinger complex; cVRG, caudal ventral respiratory group; LPfN, lateral parafacial nucleus; NTS, nucleus of the solitary tract; OFC, orbitofrontal cortex; PAG, periaqueductal gray; PB, parabrachial-Kölliker-Fuse complex; POA, preoptic area; PreBötC, pre-Bötzinger complex; RTN, retro-trapezoid nucleus; rVRG, rostral ventral respiratory group; and SC, superior colliculus. (B) Simultaneous recording of respiratory signals (top panel, monitored by a plethysmography) and ultrasonic-vocalization (USV) signal (bottom panel, shown in a spectrogram) in an adult rat during the freezing behavior. The inspiratory phase is shown in white, and expiratory phase (Exh) in gray. The figure is modified from Boulanger-Bertolus et al. (2017). Double-headed red arrows indicate a possible timing of decision making to maintain the current behavioral strategy of freezing without USV. Double-headed blue arrows indicate a possible timing of decision making to maintain the current behavioral strategy of freezing with USV. A double-headed orange arrow with a blue star indicates a possible timing of decision making to change the behavioral strategy from freezing without USV to freezing with USV. A double-headed green arrow with a red star indicates a possible timing of decision making to change the behavioral strategy from freezing with USV to freezing without USV. (C) A schematic diagram illustrating the “one respiratory cycle – one behavioral decision making” hypothesis. I, inspiratory phase; post-I, post-inspiratory phase; E1, stage 1 expiratory phase; and E2, stage 2 expiration phase. Each arrow indicates a possible timing of cortical network function in relation to one respiratory cycle.