A scent of space

Adapted from the article Follow Your Nose by Liad Hollender, Champalimaud Centre for the Unknown

A neural link between smell and space

"Odour molecules do not inherently carry spatial information. However, animals in the wild use odours for spatial navigation and memory, which allows them to locate valuable resources such as food,” said Cindy Poo, an HFSP Long-Term Fellowship awardee and the study's first author. “We wanted to understand the neural basis of these behaviours, and so we decided to study how the brain combines olfactory and spatial information."

The researchers focused on the primary olfactory cortex. "The olfactory system is unique among the senses," said the study's senior author, Zachary Mainen, a principal investigator at the Champalimaud Centre for the Unknown in Portugal and HFSP research grant alumnus. "Only olfaction has direct reciprocal connections to the hippocampal system, which is involved in memory and navigation."

Hippocampal neurons are famous for functioning as ‘place cells’. This is because each cell becomes active at a specific location within an environment. Together, these neurons encode the entire area, effectively creating a neural map of space. Hippocampal place cells, whose discovery in rats led to the Nobel Prize for Physiology or Medicine in 2014, are so reliable that scientists can tell where an animal is simply by observing their activity. 

"We know that the hippocampal system sends signals to the primary olfactory cortex," said Poo. "So we suspected that this brain region might do more than just identify different smells."

Animals use their sense of smell in combination with an internal cognitive map of their environment to perform ethnologically important behaviors such as navigation and foraging. Illustration by Diogo Martins.

Putting olfactory neurons to the test

To test this idea, the researchers developed a custom-made puzzle for rats, which are highly adept at olfaction. The rats sampled odours at the four ends of a plus-shaped maze. Then, depending on the scent, they had to figure out where the reward was hidden. "In this task, the rats had to learn and remember exact associations of odours and locations," Poo explained. 

While the animals were solving the puzzle, the researchers monitored the activity of neurons in a part of the primary olfactory cortex called the posterior piriform cortex. "Neurons communicate with one another by emitting electric impulses," explained Mainen. "By recording the electric signals emitted by hundreds of individual neurons in this brain area, we were able to decode what specific neurons cared about. For instance, whether they became active when the animal was smelling a specific odour, or when it was at a certain location in the maze."  

"Our results exceeded our expectations," said Poo. "We had predicted that some neurons here might care about location to a certain degree. "However, by carefully studying the activity of olfactory cortex neurons while the animal was navigating in the maze, we found that these neurons had learned an entire map of the environment."

Olfactory neurons encode spatial maps

The researchers discovered a large population of neurons that, similarly to hippocampal place cells, became active at a specific location in the maze. Interestingly, the map didn't cover the entire environment equally. Instead, it was largely restricted to behaviourally significant spots on the maze: where the animals experienced the odours and received rewards.

"It appears that important locations were learned through experience and encoded into a map. It was remarkable that these cells in the olfactory system started responding in a given location when no odours were present, even when the rat was just walking around and not engaged in the task,” Mainen added.

A scent of space

Is this how we come to form memories that link certain smells with specific places? "We found that some neurons here responded to smell, others to location, and yet others to both types of information to varying degrees. All these different neurons are mixed together, and are probably interconnected. Therefore, one can speculate that activating smell-space associations can happen through activity within this network," suggested Poo.  

The support of HFSP played an important part enabling the authors to set up this ambitious project, and opens up a new window to understanding how the senses are used for navigation and memory. These results will guide future work on the mechanism and function of dynamic interactions between distributed sensory and spatial memory centers in the brain.

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When a smell evokes a memory: new research offers clues about how the two are linked in the brain (The Conversation)