Amphioxus-like creatures at the beginning of vertebral life did not have heads. They were segmented all the way from tip to tail. Their spinal nerves were also not in dorsal/ventral pairs, which presumably meant that they did not have the simple spinal reflexes that our paired nerves give us. Perhaps they had a less organized way of responding to stimulus.
An evolutionary pressure to coordinate movement with sensory input must have been behind the pairing of dorsal and ventral spinal nerves. This pressure did not operate inside the evolving head, since dorsally and ventrally rooted nerves remained separate there.
Nevertheless, even in the head, a segmented body plan remained the basic template on which later variations were built. There are 8 cranial segments around which the head evolved, and 12 cranial nerves, with some dispute on exactly how to count both of these. The cranial nerves have been the least variable part of the head over evolutionary time.
Of the 8 cranial segments, the top four are for orienting the self in relation to its food source (through smell, sight, hearing, balance, and touch to the head), and for being able to take hold of food with the mouth. The bottom four are for swallowing and processing food (or air), and for positioning the head and tongue to do so.
The cranial segments are not easy to see, especially in later vertebrates like us. They are obscured by several factors:
1. Segments are most evident in embryos in the first few weeks of life, and are harder to see later.
2. In humans, the face orients frontally, more or less at right angles to the spine.This folds or rolls the segmented structure like a fiddlehead at its top end. Our head segments are thus more wedge-shaped and less like parallel slices. This also makes them hard to see.
3. Within each cranial segment over the course of the head’s evolution, an ever increasing flood of sensory input required more and more thickening of nerve tissue around the nerve roots to process what was coming in. These swellings gave rise to different parts of the brain, often engulfing the nerve nuclei and their links to their original segments.
4. Between cranial segments, the need for coordination at times required cranial nerves to take over parts of each other’s function or segmental territory.
The skull evolved as an external shell (or exoskeleton) to give stability to the special senses embedded in it. Having such a structure made the head move as a single unit. In this situation, it did not serve any purpose to have different cranial nerves supplying different skin contact areas, so a single nerve (the fourth, or trigeminal one) took over the entire function of detecting head skin contact and being able to respond defensively by biting. It thus became the largest cranial nerve, and the only one with a dermatome.
Some cranial segments have modified considerably over time. Thus, the 4th segment in fish was the nerve source for the second (hyoid) gill arch and for the balance mechanism. The muscles of this second gill arch later evolved into constrictor colli muscles in reptiles, and still later differentiated into mammalian muscles of facial expression. So although facial muscles and the balance mechanism belong to separate cranial nerves, they are still parts of the same original cranial segment, and emerge from common tissue in human embryos.
Some cranial nerves are hard to make sense of, either because they join seemingly unrelated functions into a single nerve (as in the 8th cranial nerve, which serves both hearing and balance), or because they do the opposite, separating seemingly unitary functions into several different nerve pathways (as in the 3rd, 4th, and 6th cranial nerves, which all help control eye movement, or in the 7th and 9th cranial nerves, which govern taste).
In the case of the 8th nerve, although hearing and balance seem unrelated, their mechanisms are strikingly similar, pointing to a common evolutionary source. Both probably evolved from invaginations of previously external lateral lines. The lateral lines exposed little external hairs to surrounding water movement, and connected the hair roots to nerve. Balance and hearing use the same mechanism inside enclosed canals. Hearing may have arisen from the balance sense, and may be a specialized version of it.
It is less clear why there should be three completely separate cranial nerves controlling eye movement, with two of them controlling a single muscle each. The oculomotor nerve controls all of the eye muscles that we use for convergent focus, and that a fish would use for looking ahead. The abducens nerve controls divergent eye muscles, the ones that give us panoramic peripheral vision for surveying the wider scene. The trochlear nerve would probably allow a fish to look both up and back, perhaps to protect against attack from behind. So the functions of these three sets of nerves may have originally been quite distinct: one for pursuing food, one for protecting against attack, and one for quietly looking around when neither food nor threat were present. Such a difference of function might be more profound for the organism than the fact that these functions happen to be performed by the same sensory organ.
Except for the olfactory nerve, all the nerve tracts for the special senses synapse in the thalamus before passing to the brain centers that process their sensory information. The thalamus thus serves as a kind of post office, making sure sensory information gets sent to the right brain address. The mind of the thalamus is thus one of understanding, of having a sense of where information belongs. Once the correct pathways are found, the relief experienced probably stimulates the choroid plexi on the inner side of the thalamus to release cerebrospinal fluid into the ventricles. In this way, understanding may literally nourish the brain.
Erik Bendix, 2007