Spatial Olfactory Memory and Spatial Olfactory Navigation: History
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Contributor:
Sara Invitto
,
Giuseppe Accogli
,
Mariangela Leucci
,
Marika Salonna
,
Tonia Serio
,
Francesca Fancello
,
Vincenzo Ciccarese
,
Dion Lankford

Many studies have focused on navigation, spatial skills, and the olfactory system in comparative models, including those concerning the relationship between them and physical activity.

  • spatial olfactory navigation
  • spatial representation
  • spatial memory
  • olfaction

1. Human Spatial Representation and Navigation

In humans, spatial navigation is generally regulated by three types of spatial knowledge. It is possible to distinguish between: landmarks, i.e., fixed salient features or points of reference in the environment; route knowledge, i.e., sequences of locations as experienced by the navigator, and thus associated with an egocentric reference system; survey knowledge that includes information about the general structures of routes and the spatial relationships between different sites and associated with an allocentric reference system; graph knowledge, a network of maps and places that consists of a topological connection between various locations [1][2][3][4]. Moreover, there are three strategies used in space navigation: egocentric, allocentric, and beacon. The allocentric representation (world-focused) refers to landmarks external to the navigator, while the egocentric type of representation (body-focused) implies a reference to the current body position of the individual. Beacon concerns navigation to one or more objects and requires the memory of the object itself and the ability to distinguish it from other objects and characteristics; therefore, it could be considered as an object that indicates a nearby target location or the target itself [2][5].
A neural network underlying space navigation in humans is based both on specific cells activated in response to specific spatial positions—mainly present in the hippocampal cells that respond to the sight of landmarks. The hippocampus blends spatial and visual characteristics with the context to calculate flexible representations that are similar to maps of space [6]. The hippocampus, in addition to being involved in the organization and expression of memories, is essential for space navigation [7].
In particular, the hippocampus and entorhinal cortex could contain map-like spatial codes, while the parahippocampal and retrosplenial cortex could provide the inputs that allow for cognitive maps to connect to fixed environmental reference points [8][9].
Jacobs et al. [10] have identified cells in humans with a similar activity to grid cells, which are believed to be responsible, in animals, for numerous spatial behaviors. These are mainly distributed in the entorhinal and cingulate cortices and the hippocampus.
In addition, right-lateralized brain activities have been identified in spatial navigation tasks. This allowed for researchers to hypothesize that gamma oscillations in cerebral electrical activity in the right neocortex (in particular, in the temporal, parietal, and occipital cortices) play an important role in human space navigation [11].
Furthermore, human space navigation would also seem to be influenced by age and sex [12][13][14].

2. Spatial Navigation and Olfaction in Humans

Jacobs [15] hypothesizes that the primary function of olfaction was navigation, thanks to its ability to map odorants in space, as well as to discriminate them.
In the animal kingdom, the sense of smell still plays a vital role in navigation and spatial orientation. A hippocampal region associated with spatial orientation and an olfactory–hippocampal projection is preserved in some groups of animals, such as rodents, in which the olfactory system is connected to the hippocampus through the entorhinal cortex [16]. With regard to the spatial organization, young rats are better at using the sense of smell but are less efficient at using visual information as opposed to older rats, although there is still an interaction between different sensory modalities [17]. Seabirds are able to use olfactory cues to navigate even in very large spaces, as well as to search for food [18].
However, few studies focus on the role of smell in human spatial navigation. For example, Bao et al. [19] explain how odor information can be assembled into spatially navigable cognitive maps, optimizing orientation, and pathfinding to an odor source. Dahmani et al. [20] show that particular structures of the human hippocampus (specifically the fimbria–fornix volume) are connected to both navigational learning and olfactory identification. Dahmani et al. [21] focus on how olfactory identification covaries with spatial memory and how the thickness of the left medial orbitofrontal cortex and the volume of the right hippocampus predict both olfactory identification and spatial memory. Hamburger and Knauff [22] show how humans are able to expand their cognitive map of the environment with olfactory landmarks used in spatial orientation.
Jacobs et al. [23] show that humans can use the olfactory modality to map and reorient themselves in a previously learned place. Goodrich-Hunsaker et al. [24] found that the hippocampus is essential for associative odor-place memory and spatial recognition memory, supporting the hypothesis that associative odor–place memory is mediated by the hippocampus in both rodents and humans.
This highlights that there is a lack of information regarding the connection between the olfactory modality, orientation, and spatial navigation in humans.

3. Spatial Navigation in Athletes and Non-Athletes

Spatial representation and navigation represent one of the many cognitive abilities available, and therefore they can influence human life in many contexts. In the recent literature, many studies focus on the relationship between physical activity and its impact on human cognitive abilities—including representation and space navigation—even if there is no unanimous agreement regarding the benefits of physical activity on the cognitive system [25][26].
Although a specific and clear link has not yet been identified, it is assumed that physical exercise may increase cognition indirectly, for example, by improving health and reducing chronic diseases that have a certain impact on neurocognitive functions [27][28]. Furthermore, the benefits associated with physical activity may vary based on genetic or diet-related factors [29].
Some studies report a strong influence of physical activity on brain functions—such as learning, memory, executive functions— and cognitive decline [30][31], as well as an increased volume of gray and white matter regions [32] in the hippocampus. High levels of aerobic exercise appear to be associated with a more extensive right and left hippocampus, and larger hippocampus and higher fitness levels seem to be correlated with improved spatial memory performance [33][34].
Moreover, increased physical activity appears to be linked to greater hippocampal and basal ganglia volume, greater white matter integrity in preadolescents, and greater volumes of the prefrontal cortex and basal ganglia, as well as the hippocampus, in older adults [29].
In addition, physical activity has a more significant effect on cognitive functioning and the future incidence of cognitive decline among subjects carrying at least one copy of the APOE ε4 allele [35]. It could represent an advantage in reducing the risk of Alzheimer’s disease, other forms of dementia (excluding vascular dementia), and cognitive decline [36].
There are not many studies that specifically focus on the relationship between spatial ability and athletes, I and results are often in contrast with what has been previously reported. For example, Cynthia et al. [37] reported that the spatial ability of athletes and non-athletes is not significantly different from each other, concluding that exercise may or may not increase the spatial capacity of both groups. However, specific sport skills did not further affect the spatial abilities of the athletes. Jansen and Lehmann [38] examined visual–spatial cognition in athletes and non-athletes through an object-based mental rotation task, showing that all participants had greater accuracy for the rotation of human figures than objects and only one class of the athletes considered demonstrated a better mental rotation performance than non-athletes.

4. Visual–Spatial Memory and Olfaction

The literature shows that olfaction may be related to tasks that require the use of visual–spatial memory [39][40][41].
Furthermore, some researchers hypothesized that olfactory identification and visuospatial memory would be linked by overlapping brain areas, which include the left orbitofrontal cortex and the right hippocampus [21]. Moreover, the visual–spatial component is also extremely present in the olfactory perception, where, from an evolutionary point of view, the further development of ancestral olfactory abilities is linked to the location of the olfactory marker. Evolution has favored the development of vision, leading to a decline in the olfactory sense in the human being [42].
Recently, research has focused on the link between olfactory stimuli and cognitive and physical performance in athletes [23][43][44].

This entry is adapted from the peer-reviewed paper 10.3390/brainsci12081108

References

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