The ear, the nose, the eye: all of the neurons closest to the environment are doing on thing: attempting to represent the outside world as perfectly as possible. Total perfection is not possible – you can only only make the eye so large and only need to see so much detail in order live your life. But if you were to try to predict what the neurons in the retina or the ear are doing based on what could provide as much information as possible, you’d do a really good job. Once that information is in the nervous system, the neurons that receive this information can do whatever they want with it, processing it further or turning it directly into a command to blink or jump or just stare into space.
Even though this is the story that all of us neuroscientists get told, it’s not the full thing. Awhile back, I posted that the retina receives input from other places in the brain. That just seems weird from this perspective. If the retina is focused on extracting useful information about the visual world, why would it care about how the world smells?
One simple explanation might be that the neurons only want to code for surprising information. Maybe the nose can help out with that? After all, if something is predictable then it is useless; you already know about it! No need to waste precious bits. This seems to be what the purpose of certain feedback signals to the fly eye are for. A few recent papers have shown that neurons in the eye that respond to horizontal or vertical motion receive signals about how the animal is moving, so that when the animal moves to the left it should expect leftward motion in the horizontal cells – and so only respond to leftward motion that is above and beyond what the animal is causing. But again – what could this have to do with smells?
Let’s think for a second about some times when the olfactory system uses non-olfactory information. The olfactory system should be trying to represent the smell-world as well as it can, just like the visual system is trying to represent the image-world. But the olfactory system is directly modulated depending on the needs of an animal at any given moment. For instance, a hungry fly will release a peptide that modifies how much a set of neurons that respond to particular odors can signal the rest of the brain. In other words, how hungry an animal is determines how well it can smell something!
These two stories – how the eye interacts with the motion of the body, how the nose interacts with hunger – might give us a hint about what is happening. The sensory systems aren’t just trying to represent as much information about the world as possible, they are trying to represent as much information about useful stuff as possible. The classical view of sensory systems is a fundamentally static one, that they have evolved to take advantage of the consistencies in the world to provide relevant information as efficiently as possible*. But the world is a dynamic place, and the needs of an animal at one time are different from the needs of the animal at another.
Take an example from tadpoles. When the tadpole is in a very dim environment, it has a harder time separating dark objects from the background. The world just has less contrast (try turning down the brightness on your screen and reading this – you’ll get the idea). One way that these tadpoles control their ability to increase or decrease contrast is through a neuromodulator that changes the resting potential of a cell (how responsive it is to stimuli), but only over relatively long timescales. This is not fast adaptation but slow adaptation to the changing world. The end result of this is that tadpoles are better able to see moving objects – but presumably at the expense of being worse at seeing something else. That seems like a pretty direct way of going from a need for the animal to code certain visual information more efficiently to the act of doing it. The point is not that this is driven by a direct behavioral need of the animal – I have no idea if this is due to a desire to hunt or avoid objects or what-have-you. Instead, it’s an example of how an animal could control certain information if it wanted to.
This kind of behavioral gating does occur from retinal feedback. Male zebrafish use a combination of smell and sight when they decide how they want to interact with other zebrafish. Certain olfactory neurons that respond to a chemical involved in mating signal to neurons in the retina – making certain cells more or less responsive in the same way that tadpoles control the contrast of their world (above). It appears as if the olfactory information sends a signal to the eye that either gates or enhances the visual information – the stripe detection or what-have-you – that the little fishies use when they want to court another animal.
The sensory system is not perfect. It must make trade-offs about which information is important to keep and which can be thrown away, about how much of its limited bandwidth to spend on one signal or another. A lot of the structure comes naturally from evolution, representing a long-term learning of the structure of the world. But animals have needs that fluctuate over other timescales – and may require more computation than can be provided directly in the sensory area. How else would the eye know that it is time to mate?
What this doesn’t answer is why the modulation is happening here; why not downstream?
* This is a major simplification, obviously, and a lot of work has been done on adaptation, etc in the retina.