Eyes wide shut: How newborn mammals dream the world they're entering

As a newborn mammal opens its eyes for the first time, it can already make visual sense of the world around it. But how does this happen before they have experienced sight?

A new Yale study suggests that, in a sense, mammals dream about the world they are about to experience before they are even born.

Writing in the July 23 issue of Science, a team led by Michael Crair, the William Ziegler III Professor of Neuroscience and professor of ophthalmology and visual science, describes waves of activity that emanate from the neonatal retina in mice before their eyes ever open.

This activity disappears soon after birth and is replaced by a more mature network of neural transmissions of visual stimuli to the brain, where information is further encoded and stored.

"At eye opening, mammals are capable of pretty sophisticated behavior," said Crair, senior author of the study, who is also vice provost for research at Yale." But how do the circuits form that allow us to perceive motion and navigate the world? It turns out we are born capable of many of these behaviors, at least in rudimentary form."

In the study, Crair's team, led by Yale graduate students Xinxin Ge and Kathy Zhang, explored the origins of these waves of activity. Imaging the brains of mice soon after birth but before their eyes opened, the Yale team found that these retinal waves flow in a pattern that mimics the activity that would occur if the animal were moving forward through the environment.

"This early dream-like activity makes evolutionary sense because it allows a mouse to anticipate what it will experience after opening its eyes, and be prepared to respond immediately to environmental threats," Crair noted.

Going further, the Yale team also investigated the cells and circuits responsible for propagating the retinal waves that mimic forward motion in neonatal mice. They found that blocking the function of starburst amacrine cells, which are cells in the retina that release neurotransmitters, prevents the waves from flowing in the direction that mimics forward motion. This in turn impairs the development of the mouse's ability to respond to visual motion after birth.

Intriguingly, within the adult retina of the mouse these same cells play a crucial role in a more sophisticated motion detection circuit that allows them to respond to environmental cues.

Mice, of course, differ from humans in their ability to quickly navigate their environment soon after birth. However, human babies are also able to immediately detect objects and identify motion, such as a finger moving across their field of vision, suggesting that their visual system was also primed before birth.

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How we retrieve our knowledge about the world

To understand the world, we arrange individual objects, people, and events into different categories or concepts. Concepts such as 'the telephone' consist primarily of visible features, i.e. shape and color, and sounds, such as ringing. In addition, there are actions, i.e. how we use a telephone.

However, the concept of telephone does not only arise in the brain when we have a telephone in front of us. It also appears when the term is merely mentioned. If we read the word "telephone," our brain also calls up the concept of telephone. The same regions in the brain are activated that would be activated if we actually saw, heard, or used a telephone. The brain thus seems to simulate the characteristics of a telephone when its name alone is mentioned.

Until now, however, it was unclear, depending on the situation, whether the entire concept of a telephone is called up or only individual features such as sounds or actions and whether only the brain areas that process the respective feature become active. So, when we think of a telephone, do we always think of all its features or only the part that is needed at the moment? Do we retrieve our sound knowledge when a phone rings, but our action knowledge when we use it?

Researchers at the Max Planck Institute for Human Cognitive and Brain Sciences in Leipzig have now found the answer: It depends on the situation. If, for example, the study participants thought of the sounds associated with the word "telephone," the corresponding auditory areas in the cerebral cortex were activated, which are also activated during actual hearing. When thinking about using a telephone, the somatomotor areas that underlie the involved movements came into action.

In addition to these sensory-dependent, so-called modality-specific areas, it was found that there are areas that process both sounds and actions together. One of these so-called multimodal areas is the left inferior parietal lobule (IPL). It became active when both features were requested.

The researchers also found out that, in addition to characteristics based on sensory impressions and actions, there must be other criteria by which we understand and classify terms. This became apparent when the participants were only asked to distinguish between real and invented words. Here, a region that was not active for actions or sounds kicked in: the so-called anterior temporal lobe (ATL). The ATL therefore seems to process concepts abstractly or "amodally," completely detached from sensory impressions.

From these findings, the scientists finally developed a hierarchical model to reflect how conceptual knowledge is represented in the human brain. According to this model, information is passed on from one hierarchical level to the next and at the same time becomes more abstract with each step. On the lowest level, therefore, are the modality-specific areas that process individual sensory impressions or actions. These transmit their information to the multimodal regions such as the IPL, which process several linked perceptions simultaneously, such as sounds and actions. The amodal ATL, which represents features detached from sensory impressions, operates at the highest level. The more abstract a feature, the higher the level at which it is processed and the further it is removed from actual sensory impressions.

"We thus show that our concepts of things, people, and events are composed, on the one hand, of the sensory impressions and actions associated with them and, on the other hand, of abstract symbol-like features," explains Philipp Kuhnke, lead author of the study, which was published in the journal Cerebral Cortex. "Which features are activated depends strongly on the respective situation or task" added Kuhnke.

In a follow-up study in Cerebral Cortex, the researchers also found that modality-specific and multimodal regions work together in a situation-dependent manner when we retrieve conceptual features. The multimodal IPL interacted with auditory areas when retrieving sounds, and with somatomotor areas when retrieving actions. This showed that the interaction between modality-specific and multimodal regions determined the behavior of the study participants. The more these regions worked together, the more strongly the participants associated words with actions and sounds.

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