Sensory Systems/NonPrimates

Primates are animals belonging to the class of mammals. Primates include humans and the nonhuman primates, the apes, monkeys, lemurs, tree-shrews, lorises, bush babies and tarsiers. They are characterized by a voluminous and complicated forebrain. Most have excellent sight and are highly adapted to an arboreal existence, including in some species the possession of a prehensile tail. Non primates on the other hand often posses smaller brains. But as we learn more about the rest of the animal world, it’s becoming clear that non-primates are pretty intelligent too. Some examples include pigs, octopus, and crows.

In many branches of mythology, the crow plays a shrewd trickster, and in the real world, crows are proving to be quite a clever species. Crows have been found to engage in feats such as tool use, the ability to hide and store food from season to season, episodic-like memory, and the ability to use personal experience to predict future conditions.

As it turns out, being piggy is actually a pretty smart tactic. Pigs are probably the most intelligent domesticated animal on the planet. Although their raw intelligence is most likely commensurate with a dog or cat, their problem-solving abilities top those of felines and canine pals.

If pigs are the most intelligent of the domesticated species, octopuses take the cake for invertebrates. Experiments in maze and problem-solving have shown that they have both short-term and long-term memory. Octopuses can open jars, squeeze through tiny openings, and hop from cage to cage for a snack. They can also be trained to distinguish between different shapes and patterns. In a kind of play-like activity (one of the hallmarks of higher intelligence species) octopuses have been observed repeatedly releasing bottles or toys into a circular current in their aquariums and then catching them.

Octopus

Introduction

One of the most interesting non-primate is the octopus. The most interesting feature about this non-primate is its arm movement. In these invertebrates, the control of the arm is especially complex because the arm can be moved in any direction, with a virtually infinite number of degrees of freedom. In the octopus, the brain only has to send a command to the arm to do the action—the entire recipe of how to do it is embedded in the arm itself. Observations indicate that octopuses reduce the complexity of controlling their arms by keeping their arm movements to set, stereotypical patterns. To find out if octopus arms have minds of their own, the researchers cut off the nerves in an octopus arm from the other nerves in its body, including the brain. They then tickled and stimulated the skin on the arm. The arm behaved in an identical fashion to what it would in a healthy octopus. The implication is that the brain only has to send a single move command to the arm, and the arm will do the rest.

In this chapter we discuss in detail the sensory system of an octopus and focus on the sensory motor system in this non-primate.

Octopus - The intelligent non-primate

The Common Octopus, Octopus vulgaris.

Octopuses have two eyes and four pairs of arms, and they are bilaterally symmetric. An octopus has a hard beak, with its mouth at the center point of the arms. Octopuses have no internal or external skeleton (although some species have a vestigial remnant of a shell inside their mantle), allowing them to squeeze through tight places. Octopuses are among the most intelligent and behaviorally flexible of all invertebrates.

The most interesting feature of the octopuses is their arm movements. For goal directed arm movements, the nervous system in octopus generates a sequence of motor commands that brings the arm towards the target. Control of the arm is especially complex because the arm can be moved in any direction, with a virtually infinite number of degrees of freedom. The basic motor program for voluntary movement is embedded within the neural circuitry of the arm itself.

Arm Movements in Octopus

In the hierarchical organization in octopus, the brain only has to send a command to the arm to do the action. The entire recipe of how to do it is embedded in the arm itself. By the use of the arms octopus walks, seizes its pray, or rejects unwanted objects and also obtains a wide range of mechanical and chemical information about its immediate environment.

Octopus arms, unlike human arms, are not limited in their range of motion by elbow, wrist, and shoulder joints. To accomplish goals such as reaching for a meal or swimming, however, an octopus must be able to control its eight appendages. The octopus arm can move in any direction using virtually infinite degrees of freedom. This ability results from the densely packed flexible muscle fibers along the arm of the octopus.

Observations indicate that octopuses reduce the complexity of controlling their arms by keeping their arm movements to set, stereotypical patterns. For example, the reaching movement always consists of a bend that propagates along the arm toward the tip. Since octopuses always use the same kind of movement to extend their arms, the commands that generate the pattern are stored in the arm itself, not in the central brain. Such a mechanism further reduces the complexity of controlling a flexible arm. These flexible arms are controlled by an elaborate peripheral nervous system containing 5 × 10⁷ neurons distributed along each arm. 4 × 10⁵ of these are motor neurons, which innervate the intrinsic muscles of the arm and locally control muscle action.

Whenever it is required, the nervous system in octopus generates a sequence of motor commands which in turn produces forces and corresponding velocities making the limb reach the target. The movements are simplified by the use of optimal trajectories made through vectorial summation and superposition of basic movements. This requires that the muscles are quite flexible.

The Nervous System of the Arms

The eight arms of the octopus are elongated, tapering, muscular organs, projecting from the head and regularly arranged around the mouth. The inner surface of each arm bears a double row of suckers, each sucker alternating with that of the opposite row. There are about 300 suckers on each arm.

The arms perform both motor and sensory functions. The nervous system in the arms of the octopus is represented by the nerve ganglia, subserving motor and inter-connecting functions. The peripheral nerve cells represent the sensory systems. There exists a close functional relationship between the nerve ganglia and the peripheral nerve cells.

General anatomy of the arm

The muscles of the arm can be divided into three separate groups, each having a certain degree of anatomical and functional independence:

1. Intrinsic muscles of the arm,
2. Intrinsic muscles of the suckers, and
3. Acetabulo-brachial muscles (connects the suckers to the arm muscles).

Each of these three groups of muscles comprises three muscle bundles at right angles to one another. Each bundle is innervated separately from the surrounding units and shows a remarkable autonomy.In spite of the absence of a bony or cartilaginous skeleton, octopus can produce arm movements using the contraction and relaxation of different muscles. Behaviorally, the longitudinal muscles shorten the arm and play major role in seizing objects carrying them to mouth, and the oblique and transverse muscles lengthen the arms and are used by octopus for rejecting unwanted objects.

Cross section of an octopus arm: The lateral roots innervate the intrinsic muscles, the ventral roots the suckers.

Six main nerve centers lie in the arm and are responsible for the performance of these sets of muscles. The axial nerve cord is by far the most important motor and integrative center of the arm. The eight cords one in each arm contains altogether 3.5 × 10⁸ neurons. Each axial cord is linked by means of connective nerve bundles with five sets of more peripheral nerve centers, the four intramuscular nerve cords, lying among the intrinsic muscles of the arm, and the ganglia of the suckers, situated in the peduncle just beneath the acetabular cup of each sucker.

All these small peripheral nerves contain motor neurons and receive sensory fibers from deep muscle receptors which play the role of local reflex centers. The motor innervation of the muscles of the arm is thus provided not only by the motor neurons of the axial nerve cord, which receives pre-ganglionic fibers from the brain, but also by these more peripheral motor centers.

Sensory Nervous system

The arms contain a complex and extensive sensory system. Deep receptors in the three main muscle systems of the arms, provide the animal with a widespread sensory apparatus for collecting information from muscles. Many primary receptors lie in the epithelium covering the surface of the arm. The sucker, and particularly its rim, has the greatest number of these sensory cells, while the skin of the arm is rather less sensitive. Several tens of thousands of receptors lie in each sucker.

Three main morphological types of receptors are found in arms of an octopus. These are round cells, irregular multipolar cells, and tapered ciliated cells. All these elements send their processes centripetally towards the ganglia. The functional significance of these three types of receptors is still not very well known and can only be conjectured. It has been suggested that the round and multipolar receptors may record mechanical stimuli, while ciliated receptors are likely to be chemo-receptors.

The ciliated receptors do not send their axons directly to the ganglia but the axons meet encapsulated neurons lying underneath the epithelium and make synaptic contacts with the dendritic processes of these. This linkage helps in reduction of input between primary nerve cells. Round and multipolar receptors on the other hand send their axons directly to the ganglia where the motor neurons lie.

Functioning of peripheral nervous system in arm movements

Behavioral experiments suggest that information regarding the movement of the muscles does not reach the learning centers of the brain, and morphological observations prove that the deep receptors send their axons to peripheral centers such as the ganglion of the sucker or the intramuscular nerve cords. The information regarding the stretch or movement of the muscles is used in local reflexes only.

When the dorsal part of the axial nerve cord that contains the axonal tracts from the brain is stimulated by electrical signals, movements in entire arm are still noticed. The movements are triggered by the stimulation which is provided and is not directly driven by the stimuli coming from the brain. Thus, arm extensions are evoked by stimulation of the dorsal part of the axial nerve cord. In contrast, the stimulation of the muscles within the same area or the ganglionic part of the cord evokes only local muscular contractions. The implication is that the brain only has to send a single move command to the arm, and the arm will do the rest.

A dorsally oriented bend propagates along the arm causing the suckers to point in the direction of the movement. As the bend propagates, the part of the arm proximal to the bend remains extended. For further conformations that an octopus arm has a mind of its own, the nerves in an octopus arm have been cut off from the other nerves in its body, including the brain. Movements resembling normal arm extensions were initiated in amputated arms by electrical stimulation of the nerve cord or by tactile stimulation of the skin or suckers.

It has been noted that the bend propagations are more readily initiated when a bend is created manually before stimulation. If the fully relaxed arm is stimulated, the initial movement is triggered by the stimuli, which follows the same bend propagation. The nervous system of the arm thus, not only drives local reflexes but controls complex movements involving the entire arm.

These evoked movements are almost kinematically identical to the movements of freely behaving octopus. When stimulated, a severed arm shows an active propagation of the muscle activity as in natural arm extensions. Movements evoked from similar initial arm postures result in similar paths, while different starting postures result in different final paths.

As the extensions evoked in denervated octopus arms are qualitatively and kinematically similar to natural arm extensions, an underlying motor program seems to be controlling the movements which are embedded in the neuromuscular system of the arm, which does not require central control.

Fish

Fish are aquatic animals with great diversity. There are over 32’000 species of fish, making it the largest group of vertebrates.

The lateral line sensory organ shown on a shark.

Most fish possess highly developed sense organs. The eyes of most daylight dwelling fish are capable of color vision. Some can even see ultra violet light. Fish also have a very good sense of smell. Trout for example have special holes called “nares” in their head that they use to register tiny amounts of chemicals in the water. Migrating salmon coming from the ocean use this sense to find their way back to their home streams, because they remember what they smell like. Especially ground dwelling fish have a very strong tactile sense in their lips and barbels. Their taste buds are also located there. They use these senses to search for food on the ground and in murky waters.

Fish also have a lateral line system, also known as the lateralis system. It is a system of tactile sense organs located in the head and along both sides of the body. It is used to detect movement and vibration in the surrounding water.

Function

Fish use the lateral line sense organ to sense prey and predators, changes in the current and its orientation and they use it to avoid collision in schooling.

Coombs et al. have shown [1] that the lateral line sensory organ is necessary for fish to detect their prey and orient towards it. The fish detect and orient themselves towards movements created by prey or a vibrating metal sphere even when they are blinded. When signal transduction in the lateral lines is inhibited by cobalt chloride application, the ability to target the prey is greatly diminished.

The dependency of fish on the lateral line organ to avoid collisions in schooling fish was demonstrated by Pitcher et al. in 1976, where they show that optically blinded fish can swim in a school of fish, while those with a disabled lateral line organ cannot [2].

Anatomy

The lateral lines are visible as two faint lines that run along either side of the fish body, from its head to its tail. They are made up of a series of mechanoreceptor cells called neuromasts. These are either located on the surface of the skin or are, more frequently, embedded within the lateral line canal. The lateral line canal is a mucus filled structure that lies just beneath the skin and transduces the external water displacement through openings from the outside to the neuromasts on the inside. The neuromasts themselves are made up of sensory cells with fine hair cells that are encapsulated by a cylindrical gelatinous cupula. These reach either directly into the open water (common in deep sea fish) or into the lymph fluid of the lateral line canal. The changing water pressures bend the cupula, and in turn the hair cells inside. Similar to the hair cells in all vertebrate ears, a deflection towards the shorter cilia leads to a hyperpolarization (decrease of firing rate) and a deflection in the opposite direction leads to depolarization (increase of firing rate) of the sensory cells. Therefore the pressure information is transduced to digital information using rate coding that is then passed along the lateral line nerve to the brain. By integrating many neuromasts through their afferent and efferent connections, complex circuits can be formed. This can make them respond to different stimulation frequencies and consequently coding for different parameters, like acceleration or velocity [3].

Some scales of the lateral line (center) of a Rutilus rutilus

In sharks and rays, some neuromasts have undergone an interesting evolution. They have evolved into electroreceptors called ampullae of Lorenzini. They are mostly concentrated around the head of the fish and can detect a change of electrical stimuli as small as 0.01 microvolt [4]. With this sensitive instrument these fish are able to detect tiny electrical potentials generated by muscle contractions and can thus find their prey over large distances, in murky waters or even hidden under the sand. It has been suggested that sharks also use this sense for migration and orientation, since the ampullae of Lorenzini are sensitive enough to detect the earth’s electromagnetic field.

Convergent Evolution

Cephalopods:

Cephalopods such as squids, octopuses and cuttlefish have lines of ciliated epidermal cells on head and arms that resemble the lateral lines of fish. Electrophysiological recordings from these lines in the common cuttlefish (Sepia officinalis) and the brief squid (Lolliguncula brevis) have identified them as an invertebrate analogue to the mechanoreceptive lateral lines of fish and aquatic amphibians [5].

Crustaceans:

Another convergence to the fish lateral line is found in some crustaceans. Contrary to fish, they don’t have the mechanosensory cells on their body, but have them spaced at regular intervals on long trailing antennae. These are held parallel to the body. This forms two ‘lateral lines’ parallel to the body that have similar properties to those of fish lateral lines and are mechanically independent of the body [6].

Mammals:

In aquatic manatees the postcranial body bears tactile hairs. They resemble the mechanosensory hairs of naked mole rats. This arrangement of hair has been compared to the fish lateral line and complement the poor visual capacities of the manatees. Similarly, the whiskers of harbor seals are known to detect minute water movements and serve as a hydrodynamic receptor system. This system is far less sensitive than the fish equivalent. [7]

Flies

Introduction

Halteres of the Crane fly

Halteres are sensory organs present in many flying insects. Widely thought to be an evolutionary modifcation of the rear pair of wings on such insects, halteres provide gyroscopic sensory data, vitally important for flight. Although the fly has other relevant systems to aid in flight, the visual system of the fly is too slow to allow for rapid maneuvers. Additionally, to be able to fly adeptly in low light conditions, a requirement to avoid predation, such a sensory system is necessary. Indeed, without halteres, flies are incapable of sustained, controlled flight. Since the 18th century, scientists have been aware of the role halteres play in flight, but it was only recently that the mechanisms by which they operate have been better explored.

Anatomy

The haltere evolved from the rearmost of two pairs of wings. While the first has maintained its usage for flight, the posterior pair has lost its flight functions and has adopted a slightly different shape. The haltere is visually comprised of three structural components: a knob-shaped end, a thin shaft, and a slightly wider base. The knob contains approximately 13 innervated hairs, while the base contains two chordotonal organs, each innervated by about 20-30 nerves. Chordotonal organs are sense organs thought to be solely responsive to extension, though they remain relatively unknown. The base is also covered by around 340 campaniform sensilla, which are small fibers which respond preferentially to compression in the direction in which they are elongated. Each of these fibers is also innervated. Relative to the stalk of the haltere, both the chordotonal organs and the campaniform sensilla have an orientation of approximately 45 degrees, which is optimal for measuring bending forces on the haltere. The halteres move contrary (anti-phase) to the wings during flight. The sensory components can be categorized into three groups ): those sensitive to vertical oscillations of the haltere, including the dorsal and ventral scapal plates, dorsal and ventral Hicks papillae (both the plates and papillae are subcategories of the aforementioned campaniform sensilla), and the small chordotonal organ. The basal plate (another manifestation of the sensilla) and the large chordotonal organ are sensitive to gyroscopic torque acting on the haltere, and there is also a population of undifferentiated papillae which are responsive to all strains acting on the base of the haltere. This provides an additional method for flies to distinguish between the direction of force being applied to the haltere.

Genetics

As Homeobox genes were being discovered and explored for the first time, it was found that the deletion or inactivation of the Hox gene Ultrabithorax (Ubx) causes the halteres to develop into a normal pair of wings. This was a very compelling early result as to the nature of Hox genes. Manipulations to the Antennapedia gene can similarly cause legs to become severely deformed, or can cause a set of legs to develop instead of antennae on the head.

Function

The halteres function by detecting Coriolis forces, sensing the movement of air across the potentially rotating fly body. Studies have indicated that the angular velocity of the body is encoded by the Coriolis forces measured by the halteres . Active halteres can recruit any neighboring units, influencing nearby muscles and causing dramatic changes in the flight dynamics. Halteres have been shown to have extremely fast response times, allowing these flight changes to be performed much more quickly than if the fly were to rely on its visual system. In order to distinguish between different rotational components, such as pitch and roll, the fly must be able to combine signals from the two halteres, which must not be coincident (coincident signals would diminish the ability of the fly to differentiate the rotational axes). The halteres are capable of contributing to image stabilization, as well as in-flight attitude control, which was established by numerous authors noting a reaction from the head and wings to inputs from the components of the rotation rate vector. contributions from halteres to head and neck movements have been noted, explaining their role in gaze stabilization. The fly therefore uses input from the halteres to establish where to fixate its gaze, an interesting integration of the two senses.

Mathematics

Recordings have indicated that halteres are capable of responding to stimuli at the same (double-wingbeat) frequency as Coriolis forces, the proof of concept that allows further mathematical analysis of how these measurements can occur. The vector cross-product of the halteres' angular velocity and the rotation of the body provide the Coriolis force vector to the fly. This force is at the same frequency as the wingbeat in both the pitch and roll planes, and is doubly fast in the yaw plane. Halteres are capable of providing a rate damping signal to affect rotations. This is because the Coriolis force is proportional to the fly's own rotation rate. By measuring the Coriolis force, the halteres can send an appropriate signal to their affiliated muscles, allowing the fly to properly control its flight. The large amplitude of haltere motion allows for the calculation of the vertical and horizontal rates of rotation. Because of the large disparity in haltere movement between vertical and horizontal movement, Ω₁, the vertical component of the rotation rate, generates a force of double the frequency of the horizontal component. It is widely thought that this twofold frequency difference is what allows the fly to distinguish between the vertical and horizontal components. If we assume that the haltere moves sinusoidally, a reasonably accurate approximation of its real-world behavior, the angular position γ can be modeled as: $\gamma = \frac{\pi}{ 2}\sin(\omega t)$ where ω is the haltere beat frequency, and the amplitude is 180, a close approximation to the real life range of motion. The body rotational velocities can be computed, given the known rates (the roll, pitch, and yaw components are labeled below with 1, 2, and 3, respectively) from the two halteres' (Ω_b being the left and Ω_c being the right haltere) reference frames, respective to the body of the fly with the following calculations :

$W_{1} = - \frac{\Omega_{b3} + \Omega_{c3} }{2\sin(\alpha)}$
$W_{2} = \frac{\Omega_{b3} - \Omega_{c3} }{2\cos(\alpha)}$

$W_{3} = - \frac{\Omega_{b1} + \Omega_{c1} }{2}$

α represents the haltere angle of rotation from the body plane, and the Ω terms are, as mentioned, the angular velocity of the haltere with respect to the body. Knowing this, one could roughly simulate input to the halteres using the equation for forces on the end knob of a haltere:

$F = mg - ma_{i} - ma_{F} - m\dot{\Omega_{i}}\times r_{i} -m\Omega_{i}\times (\Omega_{i}\times r_{i} ) - 2m\Omega_{i} \times v_{i}$

m is the mass of the knob of the haltere, g is the acceleration due to gravity, r_i, v_i,} and a_i are the position, velocity, and acceleration of the knob relative to the body of the fly in the i direction, a_F is the fly's linear acceleration, and Ω_i and Ώ_i are the angular velocity and acceleration components for the direction i, respectively, of the fly in space. The Coriolis force is simulated by the 2mΩ × v_i term. Because the sensory signal generated is proportional to the forces exerted on the halteres, this would allow the haltere signal to be simulated. If attempting to reconcile the force equation with the rotational component equations, it is worthwhile to remember that the force equation must be calculated separately for both halteres.

Butterflies

The sense of balance of butterflies sits at the base of the antennae.

Butterflies and moth keep their balance with Johnston's organ: this is an organ at the base of a butterfly's antennae, and is responsible for maintaining the butterfly's sense of balance and orientation, especially during flight.