Chapter 18: The Nervous System: General and Special Senses Evolution Atlas

Sense organs: Chapter 18

by Brian Wisenden

The nervous system coordinates the organ systems of the body so that the body works as an integrated whole. The nervous system gathers information from sensory neurons from sense organs, evaluates the information with associative neurons and sends appropriate responses to motor neurons. It is important that animals do this well so that they can find food, avoid predators, find and attract mates, etc, and do it better than the competition because evolution by natural selection promotes the ones that reproduce the most. Because we are all the descendants of a long line of evolutionary winners, we can safely predict that our sense organs are good at detecting stimuli.

The external world (in which food, predators and mates are found) produces important stimuli that help guide animals to appropriate behavior. The central nervous system understands only one language; the sodium-potassium depolarization across the cell membrane of a nerve cell. For the central nervous system to perceive external stimuli, sense organs must translate environmental information such as light, sound, smell, taste, touch, pressure, temperature, gravity and magnetic and electric fields into nerve impulses.

The most ancestral sensory modality is the detection of chemicals. This is largely because life began in water, the universal solvent. Chemical information is used by aquatic animals to find food, detect predators, find mates and synchronize gamete release. Aquatic animals, but terrestrial animals too (e.g. non-primate mammals), are very good at detecting chemical cues. Chemoreceptors are a sensible start to a discussion of the evolution of sensory organs.

Chemoreceptors

Chemoreceptors detect small chemical changes in the surrounding medium. The first situation to come to mind is chemicals in the external environment detected by smell or taste receptors. However, there are also chemoreceptors specialized for chemical monitoring of internal body fluids. Smell, or olfaction, is usually accomplished by receptors located in the nose region. Taste, or gustation, is usually achieved by receptors in and around the mouth. Internal chemoreceptors detect among other things, changes in pH, oxygen and carbon dioxide in blood and regulate circulatory and respiration rates.

Olfaction

Olfactory receptors are specialized neurons to detect odorants. They are similar in all vertebrates, indicating that these structures evolved early in vertebrate evolution and have been conserved ever since. The epithelial lining of receptor sites is covered with non-motile cilia (providing high surface area) at the tip of receptor cells. Chemical stimuli (i.e., odorants) dissolve into the mucus on the cilia and chemically trigger the odorant-specific receptors to initiate a nerve impulse.

In fishes, the olfactory organ is a blind sac or a loop with incurrent and excurrent openings. Lungfishes re-routed the nares to connect the external (incurrent) nares with the mouth cavity. These channels, used for air breathing, are called choanae. The choanae lengthened during reptilian evolution with the development of the secondary (hard) palate (Kardong fig 17.10, p662). In mammals, the choanae become expanded into nasal cavities and house turbinate bones that warm, moisten, clean and smell inhaled air on its way to the lungs (Pough et al. fig 17-11, p496). Olfactory receptors are also a large part of the chemical assessment of food. Odorants from food waft up to the nasal cavity during chewing.

Most vertebrates have a vomeronasal organ (= Jacobson’s Organ) located in the roof of the mouth (Kardong fig 17.13, p663). This patch of chemical receptors receives chemical information as the tongue passes over it. This is what snakes are doing when they repeatedly flick their tongue. The forked tongue of a snake allows it to smell in stereo. The vomeronasal organ detects sex pheromones and scent markings. It is found in all terrestrial vertebrates except birds, primates, turtles, and crocodiles. In non-primate mammals vomeronasal organs are cul-de-sacs that connect to the front of the mouth through nasal palatine ducts. It is not known why primates do not have them.

Gustation

Taste receptors are less sensitive than olfactory receptors both in threshold concentration and in the range of stimuli detectable. There are four basic flavors: sweet, sour, salty and bitter. Receptors specialized for each stimulus type are sequestered in taste buds in the oral cavity and pharynx (Kardong Fig 17.15 p664). Taste buds also occur in the skin of some fish (Liem et al. fig 12-5, p403) .

Mechanoreceptors

Mechanoreceptors detect deformation of the plasma membrane of a neuron or receptor cell. Some mechanoreceptors are simple and general, others are more complex and specialized for specific types of stimuli.

Each vertebrate group has mechanoreceptors for particular stimuli specific to their needs. Listing them all would distract from the focus of this module, which is to trace the evolution of human form and function.

Free (naked) endings of sensory nerves are found in all vertebrates. They are the most primitive mechanoreceptor, and the only kind found in the jawless fishes (Agnatha). They are found at the base of all mammalian hair.

Encapsulated endings are diverse among terrestrial vertebrates. They are formed by a nerve ending and a capsule of epithelial-like connective tissue. Meissner’s corpuscles detect touch and are found only in the tactile, hairless areas of primates (hands, feet).

As noted in the section on the evolution of the integument, lizards have mechanoreceptors distributed over the surface of the body in apical pits at the posterior free borders of scales. Often a hair-like filamentous bristle, called a protothrix, extends to the surface. This bristle is tactile in function. It is commonly thought that proliferation of these bristles provided thermal insulation and led to the evolution of hair during the reptile-mammal transition.

Neuromasts

Neuromasts are fundamental mechanosensory structures that form the critical sensory apparatus for detecting a wide array of external stimuli. A neuromast is a patch of hair cells embedded in a gelatinous mass called a cupula (Martini et al fig 18-12 c, p458). A hair cell has a bundle of non-motile cilia ("hairs") of varying lengths called stereocilia extending from its surface. When stereocilia are deflected the cell is stimulated to initiate a neural impulse to the brain. Steroecilia are not al the same length. The longest cilium, located at one end of the bundle, is known as the kinocilium. The other cilia are of variable length and are known as stereocilia. Neuromasts form the basic component of the lateral line system of fishes, the vestibular apparatus in the inner ear, and the auditory system.

Lateral line receptors (Fig 17.32, p678 Kardong) only function under water. Vertebrates that secondarily have returned to life in the water (e.g. aquatic mammals) do not have them. The lateral line is a canal that runs below the skin surface of the head and sides of fish and larval amphibians. The canals have small pores spaced along their length. Neuromasts are located inside the canal. Any small pressure wave, or water current displaces the fluid within the canal to be displaced that in turn stimulates the hair cells of the neuromast. Fish use their lateral line to detecting prey and maintain school formation (even in complete darkness).

Terrestrial vertebrates such as humans do not have a lateral line system. However, the system deserves mention because it is important to realize that these cells have been maintained over evolutionary time by uses in addition to the ones used by humans.

Vestibular Organs

Vestibular organs are modified neuromasts located in the inner ear that detect changes in orientation, i.e., balance and acceleration. The organ is a "labyrinth" of hollow loops filled with fluid. The loops curve to form a half-circle and they are commonly referred to as semi-circular canals. When the body changes position (e.g. rotation) fluid inside the loops lags behind. The difference in speed between the labyrinth structure and the inner fluid is detected by hair cells located at the base of each loop. The canals are aligned in different planes in 3-D space so that rotational motion stimulates each canal to a different degree thereby informing the brain about the nature of motion.

In addition to semicircular canals, there are enlarged membranous sacs at the base of the vestibular organ, in which reside maculae. Maculae are modified neuromasts comprising a patch of hair cells covered by a gelatinous sheet. The gelatinous material is often embedded with CaCO₃ crystals, called otoliths. When the head tilts gravity pulls on the crystals and bends the underlying hair cells. Maculae inform the brain about balance and about sudden changes in speed (acceleration).

Over evolutionary time the vestibular organ has become more organized and complex. Hagfish are the most primitive extant vertebrate. They are one of the jawless, limbless fishes. Hagfish have only one semicircular canal and one membranous sac. Lamprey are representative of a separate class of vertebrates that evolved separately from the hagfish line for about 400 million years. Lamprey are also jawless and limbless too but they have two semicircular canals and one membranous sac. All gnathostomes (jawed vertebrates from fish to mammals) have three semicircular canals roughly oriented in the planes of 3-D space, and two membranous sacs (Kardong p680, fig 17.34, Kardong p682, fig 17.36d). The sacs are called the utriculus and the sacculus.

Auditory role of the labyrinth and the evolution of the cochlea (inner ear)

Sound stimuli are an important source of information about the environment. Fishes use differential movement of otoliths to detect sound. Fishes in the superorder Ostariophysi (minnows, catfish, characins, suckers, in total about 64% of all freshwater fish species) use specialized ribs of trunk vertebrae #1-5 to join the swim bladder to the labyrinth. The swim bladder acts as a resonating chamber and greatly increases the range of sound stimuli these fishes can detect. Fishes have non-directional sound detection. In fishes, maculae near a region called the lagena respond to sound. The lagena is an outpocketing of the sacculus.

Amphibians detect sound by maculae in two sites in the sacculus called the amphibian and basilar papillae. Amphibians use a tectorial membrane instead of cupulae to translate sound energy to the hair cells. A tectorial membrane is a raised layer of tissue that impinges on the hair cells.

In reptiles (and birds) the lagena becomes a prominent sac suspended from the sacculus. The basilar papilla becomes incorporated into the epithelial lining now called the organ of Corti. The organ of Corti is the sole receptor for sound in crocodiles, birds, and monotremes.

In placental mammals, including humans, the lagena is greatly elongated and coiled to form the cochlear duct (or scala media). The organ of Corti is located on the epithelial floor. Perilymphatic spaces are expanded into the scala vestibuli and the scala tympani. This is the evolutionary path that gave the human cochlea three compartments: the scala media, the scala vestibuli, and the scala tympani.

Middle Ear (cavum tympanum / tympanic cavity):

Jaws evolved when the first pharyngeal (gill) arch advanced to the mouth margin and served as a hinged gate for the beginning of the digestive tract. The gill tissue associated with the first gill arch was lost. The gill slit that followed that gill arch did not completely disappear. Modern day sharks (Chondrichthyes) have a pair of small openings between the eyes and gill slits called the spiracle. The spiracle is a remnant of the gill slit of the arch that formed the jaws. The gill slits remain in communication with the pharynx of adult vertebrates and it is known as the auditory tube or the eustachian tube. The middle ear is an extension of the eustachian tube. When we "pop" our ears when flying or SCUBA diving we are re-establishing the pressure in the middle ear so that pressure on both sides of the tympanum is equal.

The middle ear contains small bones that translate sound stimuli from the external tympanum to the vestibular apparatus. Amphibians have only one middle ear ossicle; the columella (= stapes). Reptiles and birds have two middle ear ossicles; the columella (= stapes) and, you guessed it, the extracolumella (= extrastapes) (Kardong fig 17-41c, p687). During the reptile-mammal transition the bones involved in the articulation of the jaw to the skull shifted. Two small bones, the articular and the quadrate, were liberated from the jaw joint. These bones were conveniently located to serve as middle ear ossicles. Instead of disappearing over time, they became the malleus and the incus (Liem et al. p696, fig 22-2).

The outer ear

Fishes have neither an outer ear nor a tympanum. An outer ear would create too much drag friction under water. Sound stimuli travel much more efficiently through water than air therefore there is not much selection for a tympanum in aquatic vertebrates. Amphibians (frogs and toads only) were the first to live out of the water and the first to innovate a tympanum. A tympanum helps frogs hear their prey, their predators, and courtship calls from their own species. Salamanders and newts do not vocalize. The tympanum of frogs, toads, turtles, and primitive lizards is located flush with the surface of the head. In specialized lizards, crocodiles, birds and mammals the tympanum is at the end of external auditory meatus. Terrestrial mammals have extensions of fibrocartilage (auricles or pinna) to collect and orient to sound.

Photoreceptors

Photoreceptors detect light. In pre-vertebrate times, light detection meant the detection of day versus night, the passing of a shadow over the animal, and seasonal variation in photoperiod. An image-forming eye, for all its complexity, has been present from the beginning of vertebrate evolution. Although the image-forming eye sees all the same things that a primitive light receptor does, the neural wiring is different. The functions of basic light receptors are sufficiently important for them to be retained over evolutionary time.

Median eyes are ancient and widespread among vertebrates. A skull foramen occurs on the top of the skull in the jawless ostracoderms (extinct), the placoderms (extinct), the early sharks (Chondrichthyes), the early bony fishes, the early amphibians, and the early reptilies. Lamprey have a "pineal eye" located on the dorsal region of their head. Median eyes trigger physiological responses to changes in light levels (e.g. degree of pigmentation, metamorphosis, and reproductive activity). The pineal eye persists throughout vertebrate evolution (Fig 17.29, kardong p674). The pineal gland of mammals (and humans) is directly homologous to these ancient light detectors. Pineal glands are no longer perched atop the skull. Instead the pineal gland is found deep within the brain. Neurons connect the image-forming eye to the pineal gland to inform the pineal gland of day and night and seasonal changes in day length. The pineal gland is an endocrine organ that secretes melatonin, especially at night. The activity of the pineal gland is inhibited by the eyes during the day. Melatonin is important for maintaining the circadian (circa = about, dies = day) rhythms that regulate our sleep cycle. Melatonin pills, taken just before going to bed can reset the body’s internal clock by mimicking the action of the pineal gland. Thus, jet lag can be ameliorated. Melatonin has been implicated (by pharmaceutical companies mostly) as giving a boost to the immune system, and for delaying aging.

Image - forming eyes

All vertebrates have a pair of image-forming eyes. Two eyes allow for depth perception. The subphylum Cephalochordata (e.g. Amphioxus) within the phylum Chordata are the group of animals that are the most similar to the first vertebrates (phylum Chordata, subphylum Vertebrata) without actually being vertebrates. Amphioxus have ciliated photoreceptive cells in the lumen of its central nervous system (the dorsal hollow nerve cord). These cells are homologous to rod and cone photoreceptors of vertebrate eyes. It is hypothesized that an evagination of this region brought photoreceptor cells closer to the body surface. This is why the optic nerve in humans is not a nerve at all, but an extension of the brain. Surrounding tissue proliferated around the photoreceptor cells to form a wall with the receptors at the bottom of a pit. This arrangement gives the animal some ability to localize the source of light stimuli. A transparent cap over the pit would help keep it free of silt and debris and bend incident light rays to form crude shapes. Over time, natural selection would favor individuals whose photosensory pits that were best able to discern a crude image. A lens of firm transparent material positioned in the center of the pit lumen would help focus light rays on the pit bottom. Because of the huge selective benefits of vision, selection would rapidly lead to the evolution of a vertebrate eye. The same process occurred independently within octopus and squid (Phylum Mollusca, Subphylum Cephalopoda) with the evolution of an image-forming eye almost identical in structure to that of vertebrates (Pough et al. p68, fig 3.11).

In aquatic environments incident light does not bend very much as the water-cornea interface because the densities of both materials are similar. Almost all of the focusing is done by the lens. The lens of fishes is virtually spherical for maximum light-bending properties (Kardong p668, fig 17.20). To focus, muscles attached to the lens to shift the position of the lens (Kardong p669, fig 17.22). Interestingly, snakes shift their lens position to focus, suggesting they had an aquatic period in their evolution. In air, the difference in densities at the air-cornea interface causes incident light rays to bend considerably. Relatively little amount of bending is done by the lens. For this reason, the lens in humans is relatively flat. Focussing is achieved by stretching and relaxing tension on the lens to change its shape. Figs sources

Kardong KV. 2002. Vertebrates: comparative anatomy, function, evolution. 3^rd ed. McGraw Hill.

Liem et al. 2001. Functional anatomy of the vertebrates: an evolutionary approach. 3^rd ed. Harcourt.

Pough et al. 2002. Vertebrate Life. 6^th ed. PH

Bond CE 1996. Biology of fishes 2^nd ed. Saunders.