The fluid dynamics of canine olfaction: unique nasal airflow patterns as an explanation of macrosmia

Abstract

The canine nasal cavity contains hundreds of millions of sensory neurons, located in the olfactory epithelium that lines convoluted nasal turbinates recessed in the rear of the nose. Traditional explanations for canine olfactory acuity, which include large sensory organ size and receptor gene repertoire, overlook the fluid dynamics of odorant transport during sniffing. But odorant transport to the sensory part of the nose is the first critical step in olfaction. Here we report new experimental data on canine sniffing and demonstrate allometric scaling of sniff frequency, inspiratory airflow rate and tidal volume with body mass. Next, a computational fluid dynamics simulation of airflow in an anatomically accurate three-dimensional model of the canine nasal cavity, reconstructed from high-resolution magnetic resonance imaging scans, reveals that, during sniffing, spatially separate odour samples are acquired by each nostril that may be used for bilateral stimulus intensity comparison and odour source localization. Inside the nose, the computation shows that a unique nasal airflow pattern develops during sniffing, which is optimized for odorant transport to the olfactory part of the nose. These results contrast sharply with nasal airflow in the human. We propose that mammalian olfactory function and acuity may largely depend on odorant transport by nasal airflow patterns resulting from either the presence of a highly developed olfactory recess (in macrosmats such as the canine) or the lack of one (in microsmats including humans).

Figure 1.

The canine nasal airway. (a) Three-dimensional model of the left canine nasal airway, reconstructed from high-resolution MRI scans. (b) The olfactory recess is located in the rear of the nasal cavity and contains scroll-like ethmoturbinates, which are lined with olfactory epithelium. The olfactory (yellowish-brown) and respiratory (pink) regions shown here correspond to the approximate locations of sensory (olfactory) and non-sensory (squamous, transitional and respiratory) epithelium, respectively (Craven et al. 2007).

Figure 2.

The canine olfactory recess. (a) A sagittal section of the canine nasal airway reveals a peripherally located olfactory recess excluded from the respiratory part of the nose by a bony horizontal plate, the lamina transversa. This anatomical feature is characteristic of keen-scented (macrosmatic) animals and influences olfactory airflow patterns and odorant transport. Scale bar 2.5 mm. (b) For comparison, a sagittal view of the human nasal airway demonstrates the absence of an olfactory recess in the human nose (courtesy Hornung 2006). Here, the delineation of the olfactory region is as illustrated by Lang (1989). As shown by Morrison & Costanzo (1990, 1992), the shift from respiratory to olfactory epithelium is not uniform or well defined, but rather is characterized as having a mixed and irregular boundary, where clusters of olfactory cells are found among non-olfactory cells. The olfactory region shown here corresponds to the approximate location of the olfactory epithelium. Yellowish-brown, olfactory region; pink, respiratory region.

Figure 3.

Experimental measurements of canine sniffing. (a) Schematic of the experimental technique. (b) A photograph of the inlet to the specially designed muzzle used for time-accurate airflow measurements of canine sniffing.

Figure 4.

Experimental results from airflow measurements of canine sniffing. (a) Sample measurements for three dogs of widely different body size reveal the size-dependent variation of airflow rate for canine sniffing. Here, short sniffing bouts are shown that consist of a single burst of sniffs. (b) Longer bouts of sniffing typically contained multiple bursts of sniffs occurring in the 0.5–1.5 Hz range. (c) A plot of the normalized power spectral density (PSD) of sniffing calculated via a fast Fourier transform (FFT) of the time-dependent airflow rate data. For comparison, each PSD spectrum is normalized by the maximum PSD. Red lines, Pomeranian (6.8 kg); green lines, sheltie–husky mix (14.5 kg); blue lines, German shepherd (34.5 kg); black lines, Labrador retriever (52.9 kg).

Figure 5.

Scaling of the airflow variables of canine sniffing extracted from the time-dependent experimental data. (a) Frequency, (b) mean inspiratory airflow rate, (c) peak inspiratory airflow rate and (d) inspiratory tidal volume of canine sniffing versus body mass. (b–d) Scaling relationships, calculated as linear regressions of the log-transformed data, include the 95% confidence interval of the allometric exponents. Error bars represent (a) ±1% and (b–d) ±10% experimental uncertainty. Variability in the flow rate and tidal volume data is attributable to the observed rhythmic modulation of sniff airflow rate within a burst of sniffs and to the range of sniff intensities measured in response to multiple scent sources and variable odour concentration. Mean values for the rat (Youngentob et al. 1987; Charles River Laboratories 2009) and human (Vanderburgh et al. 1995; Hornung et al. 2001; Hornung 2006) are included for comparison. (b) , r²=0.92; (c) , r²=0.93; (d) ∀_insp.=2.15M^{0.99 ± 0.04}, r²=0.87.

Figure 6.

The external fluid dynamics of canine olfaction. (a) At peak inspiration, an isosurface of velocity magnitude (10% of maximum inspiratory velocity) reveals the aerodynamic reach of the left nostril, which is approximately 1 cm and smaller than the internostril separation. This airflow pattern provides bilateral odour samples that may be used by the dog for odour source localization. (b) At peak expiration, an isosurface of velocity magnitude (10% of maximum expiratory velocity) shows a ventral-laterally directed air jet containing two large co-rotating vortices expelled from the canine nose, which augments odorant collection.

Figure 7.

The intranasal fluid dynamics of canine olfaction. (a) Unsteady pathlines generated from trajectories of neutrally buoyant particles released from the naris at equally spaced time intervals throughout inspiration reveal distinct respiratory and olfactory flow paths within the nasal cavity. (b) The same inspiratory pathlines coloured by velocity magnitude show high-velocity olfactory airflow travelling back through the dorsal meatus and low-velocity airflow filtering through the olfactory recess in the forward–lateral direction. (c) Expiratory pathlines originating from the nasopharynx demonstrate that airflow bypasses the olfactory recess during expiration, leaving quiescent scent-laden air there, providing an additional residence time for enhanced odorant absorption. (a) Red lines, olfactory pathlines; blue lines, respiratory pathlines.