Decoding Odor Mixtures in the Dog Brain: An Awake fMRI Study

Abstract

In working and practical contexts, dogs rely upon their ability to discriminate a target odor from distracting odors and other sensory stimuli. Using awake fMRI in 18 dogs, we examined the neural mechanisms underlying odor discrimination between two odors and a mixture of the odors. Neural activation was measured during the presentation of a target odor (A) associated with a food reward, a distractor odor (B) associated with nothing, and a mixture of the two odors (A+B). Changes in neural activation during the presentations of the odor stimuli in individual dogs were measured over time within three regions known to be involved with odor processing: the caudate nucleus, the amygdala, and the olfactory bulbs. Average activation within the amygdala showed that dogs maximally differentiated between odor stimuli based on the stimulus-reward associations by the first run, while activation to the mixture (A+B) was most similar to the no-reward (B) stimulus. To clarify the neural representation of odor mixtures in the dog brain, we used a random forest classifier to compare multilabel (elemental) vs. multiclass (configural) models. The multiclass model performed much better than the multilabel (weighted-F1 0.44 vs. 0.14), suggesting the odor mixture was processed configurally. Analysis of the subset of high-performing dogs’ brain classification metrics revealed a network of olfactory information-carrying brain regions that included the amygdala, piriform cortex, and posterior cingulate. These results add further evidence for the configural processing of odor mixtures in dogs and suggest a novel way to identify high-performers based on brain classification metrics.

Central nodes of canine functional brain networks are concentrated in the cingulate gyrus

“…Areas across the anterior (GI, XMII), medial (LM) and posterior (LPDI, LPVI, LPVII) cingulate gyrus are all found among the most central nodes, next to the prorean gyrus and splenial gyrus. Functional dog fMRI studies also report the involvement of the cingulate gyrus across several tasks, such as word detection and odour discrimination (Prichard et al 2018(Prichard et al , 2020 The cingulate cortex plays a central role in various functions related to behavioural flexibility, ranging from autonomic regulation to action selection and performance monitoring. It is a processing hub for the regulation of autonomic responses, assessing emotional and motivational aspects of internal and external information (seeing emotional faces or listening to emotionally charged et al 2020).…”

“…Functional dog fMRI studies also report the involvement of the cingulate gyrus across several tasks, such as word detection and odour discrimination (Prichard et al. 2018 , 2020 )…”

Canine Olfaction: Physiology, Behavior, and Possibilities for Practical Applications

“…One of the advantages of fMRI is the possibility of obtaining a detailed evaluation of the brain’s reaction to a mixture of odors or to identify the particular brain region(s) activated by odors connected with some features (e.g., familiar or unfamiliar odor), studies that would be difficult to carry out using traditional, behavioral methods of examination [ 194 ].…”

“…Since behavioral reactions are very often ambiguous and difficult to interpret, new methods to evaluate the impact of odors on the chemical signal-receiver are still being proposed. In cases where a strong behavioral reaction is not advisable, such as during EEG or fMRI studies requiring long immobilization, dogs must be trained to not react to the odors presented, since reaction of the particular brain regions is interpreted as a reaction to the olfactory signal [ 62 , 193 , 194 ].…”

Non-invasive canine electroencephalography (EEG): a systematic review

“…An understanding of the neural correlates of olfaction would be vital to a greater understanding of a dog's perception and cognition. Early studies that measured EEG of sedated dogs showed promise in decipherable differences between evoked potentials between stimuli [40] and multiple studies using fMRI have observed meaningful neural correlates from olfactory tasks in dogs [50,89,90].…”