How does our brain’s activity shape behavior?

Suppose you have a ritual of eating cereal every morning for breakfast. Normally, you walk into the kitchen and perform a sequence of fine motor commands, like shaking out the proper amount of cereal, grabbing a single spoon from the drawer, pouring in milk, and carefully raising the spoon to your mouth, being mindful not to spill. But on this morning, you find no cereal in the usual spot in the cabinet. Maybe the cereal box was left on the table? Or is it in the pantry? Is there other food on the shelf I could eat instead?

On your typical morning, we might describe your behavior as exploitation. Since food was present exactly where you thought it would be, we might conclude that your brain’s activity is in a state that supports the fine motor movements needed to optimally shovel Crispix morsels into your mouth so you can get on with your day. But on that unspeakable morning when no cereal was found, your behavior switched into exploration. Food was not found in the usual spot, so you had to start a more general search for breakfast. Perhaps this required more gross motor skills as you move to search more areas. Exploitation and exploration are two examples of what scientists call an internal state, a pattern of brain activity associated with a particular mood or state of mind.

Figure 1:In the top row, color corresponds to the number of neurons observed across animals that are correlated with (top left) an exploitation state, characterized by finer locomotion that improves hunting abilities, or (top right) an exploration state, characterized by swimming across long distances in search of food. The bottom row visualizes the same data, but only including neurons that are statistically significant.

In Marques, Li, et al. (Nature 2019), the authors study how these two internal states are represented by the brain and how they change behavior. Although many of us are interested in how these states are represented in the human brain, mammalian brains, are enormous and require invasive techniques to observe even small fractions of the brain through the skull. In contrast, zebrafish, during the first two weeks of life, are transparent and small. The authors use an innovative imaging technique called DIFF imaging to see the electrical activity of every single neuron in the larval zebrafish brain while it freely swims around hunting its favorite breakfast, the single-cell organism paramecium. The authors observe that, roughly speaking, the brain activity clusters into one of two states. Much of the difference between these two states comes from the activity in the dorsal raphe, a brain region known for its serotonergic neurons that are thought to play an important role in mood and depression. When the dorsal raphe is active, the authors find that zebrafish are much more likely to converge their eyes and pursue a paramecium. Subsequently, the fish have a relatively high success rate for getting the prey in their mouth and swallowing it. Thus, the authors conclude that this first state corresponds to exploitation. In the second state, the authors observe a much lower rate of eye convergence, pursuit, and prey capture but a higher rate of locomotion. Therefore, the authors call this state exploration.

Having identified a brain region whose activity was highly correlated with behavioral state, the authors then asked the question of if particular brain regions may be implicated in switching the animal’s behavioral state from exploration to exploitation or vice versa. They found a small group of neurons in the Habenula, an area of the brain associated with reward processing, and neurons in the Rhombencephalon, the developmental predecessor to the hindbrain that are active during the transition from exploration to exploitation. This is exciting as the observation suggests that activation of these neurons may cause the fish to switch from one state to the other. Could this be a general principle of how our brains switch between different motivational states or even moods?

While rodents, primates, and humans have been shown to exhibit trade-offs between exploitation and exploration, a global alternation between two states was previously only been observed in the small nematode (worm) C. elegans. This paper suggests that during the complex task of foraging, this basic strategy of alternating between exploitation and exploration may be the principal axis of brain activity in vertebrates, too.

https://www.nature.com/articles/s41586-019-1858-z

Edited by Manasi Iyer