Cockroach antennae have been extensively used for studying the multifunctional sensory appendage that generates the olfactory, gustatory, tactile, thermal, and humidity senses. Of the variety of senses, the tactile sense is thought to play a key role for perceiving physical objects. Because most of the cockroach species are nocturnal, the tactile sense of the antenna would be essential to determine the position, shape, and texture of surrounding objects in the dark. Mechanoreceptors on the surface of the antenna are primarily responsible for the generation of tactile sense. In addition, the motor function of antenna also contributes to the active tactile sense (Staudacher et al. 2005). The antennal movement is accompanied by the activation of proprioceptors at the antennal joints.
Cockroach antenna as a tactile sense organ
Cockroaches are insect species that are classified into the order Blattaria. Currently, over 4,000 species have been found in Blattaria, but of these, only a few are known to be pests. Because these species can tolerate the human environment, and are easily reared in laboratories, they are often used for various biological studies. Presumably, Periplaneta americana, which is also known as the American cockroach, can be considered as the most representative species used for studying the antennal system.
The antenna of adult P. americana is as long as its body length (≈ 40 mm), and consists of approximately 140 segments (Figs. 1, 2). The first and second proximal segments are called the scape and the pedicel, respectively, and the remaining distal segments are collectively referred to as the flagellum. Each segment is connected to the neighboring segments via flexible joints. However, only the head-scape and scape-pedicel joints can move actively with muscle contraction. The other joints connecting the flagellar segments are deflected only passively. On the surface or beneath the cuticle of the antenna, there are numerous sensory units called sensillum. Some types of sensilla serve as mechanoreceptors that mediate the tactile sense.
Cockroach antennae have a variety of mechanoreceptors that differ in morphology, location, and function. Morphologically, the antennal mechanoreceptors are classified as follows: hair sensillum (or simply hair), campaniform sensillum, and chordotonal sensillum. The hair and campaniform sensilla are widely distributed on the surface of the antenna, whereas the chordotonal sensilla are located in the pedicel. Functionally, these mechanoreceptors are classified as exteroceptor and proprioceptor, i.e. the external and internal sensors, respectively.
Hair sensilla are frequently found on the surface of the flagellum. Each of the mechanosensitive hairs in the flagellum contains a single mechanoreceptor and several chemoreceptor cells as well. Such multifunctional hairs with relatively thick and long shafts (>50 μm in length) are termed the sensilla cheatica or cheatic sensilla (the most prominent type of bristles, as shown in Fig. 3). Each hair possesses a pore at the tip, which acts as a passage for molecules, and a flexible socket for passive deflection. The cell body (or perikaryon) of the mechanoreceptor beneath the socket is bipolar-shaped, and extends a dendrite distally to the base of the hair, and an axon proximally to the central nervous system. The dendrite contains longitudinally arranged sensory cilia (axoneme), and also a tightly packed microtubule structure (tubular body) at its tip. Deflection of the mechanosensory hair may deform the tubular body, and consequently lead to the generation of electrical signals in the receptor cell via mechano-electric transduction. The action potentials appear only transiently upon the deflection of the hair, indicating the phasic (rapidly adapting) nature of the receptor (Hansen-Delkeskamp 1992).
Campaniform sensilla are hairless mechanoreceptors located at each flagellar segment and the pedicel. They are characterized by elliptical depression of the cuticles with a dome-like upheaval (Fig. 4) or a pea-like protrusion (the latter is also called the marginal sensillum). Beneath the cuticle, there exists a single mechanoreceptor cell along with its accessory structures whose morphology is similar to the mechanosensitive hair. Each flagellar segment possesses several campaniform sensilla at both the distal and proximal margins. In P. americana, approximately 28 campaniform sensilla are arranged circularly around the distal margin of the pedicel (Toh 1981). The campaniform sensilla are presumably activated when the adjacent cuticular structures are under stress. Therefore, the extent of flexion at the antennal joints is speculated to be monitored by the campaniform sensilla. In this regard, they may function as proprioceptors.
Chordotonal sensilla are internal mechanoreceptors that serve as exteroceptors or proprioceptors. There are two different types of chordotonal sensilla inside the pedicel of P. americana: the connective chordotonal organ (or simply chordotonal organ) (Fig. 5) and Johnston's organ, which consist of 50 and 150 sensory units designated as the scolopidia, respectively (Toh 1981). The morphology of a scolopidium is characterized by the presence of a scolopale cell and an attachment cell that surrounds the dendrites of the receptor cell. The tip of the dendrite is covered by a cap (a secreted matter from the scolopale cells). The attachment cell connects the distal part of the scolopidium to the inner surface of the cuticle. Each scolopidium consists of two and three bipolar receptor cells in the chordotonal and Johnston’s organs, respectively. The chordotonal organ may function as a proprioceptor for the scape-pedicel joint (Ikeda et al. 2004). On the other hand, Johnston’s organ is rather thought to be an exteroceptor for detecting sound or substrate vibration, considering its function in other insect species.
Hair plates are clusters of the pure mechanosensory hair located at the base of an antenna. Each of the hairs contains a single mechanoreceptor cell beneath the cuticle. Several tens to over 100 hairs (15−60 μm in length) are arranged in the form of arrays adjacent to the head-scape and scape-pedicel joints (Okada and Toh 2000) (Figs. 2, 6). At first, the hair plates seem to act as exteroceptors, but they actually function as proprioceptors for the active movements of the antennal basal joints. As the joint moves, a portion of the mechanosensory hairs is deflected by the joint membrane (Fig. 6). The receptor cells of the antennal hair plates in P. americana are known to be of a tonic-phasic type with a very slow adapting nature (Okada and Toh 2001).
Antennal muscles and their innervation
The cockroach antennae are controlled by five functionally different muscles located inside the head capsule and the scape (Fig. 7, left side). The muscles in the head capsule span between the tentorium (an internal skeleton) and the proximal ends of the scape. The adductor muscle rotates the scape medially around the head-scape joint, while the abductor muscle rotates the scape laterally. The levator muscle lifts the scape vertically. The other two muscles in the scape span between the proximal ends of the scape and those of the pedicel: the levator and depressor muscles deflect the pedicel dorsally and ventrally, respectively, around the scape-pedicel joint. These five muscles are individually innervated by the antennal motor nerves arising from the brain (Fig. 7, right side). Each antennal muscle may be innervated from 2−3 excitatory motor neurons (Baba and Comer 2008). It has also been suggested that some antennal motor nerves contain axons from a single inhibitory motor neuron (common inhibitor neuron) and dorsal unpaired median (DUM) neurons (Baba and Comer 2008). The DUM neuron is considered to be responsible for releasing an excitatory modulator substance, possibly octopamine, to the antennal muscles.
The output pattern of the antennal motor neurons has hardly been recorded across the insect species probably because of the difficulty to generate their activities under the physiological experimental conditions. However, it has recently been reported in P. americana that pilocarpine, a plant-derived muscarinic agonist, effectively induces the rhythmic bursting activities of antennal motor neurons even in isolated brain preparations (Okada et al. 2009). The drug-induced output pattern is coordinated among the five antennal motor nerves. An agonistic pair of the motor nerves (3 vs. 4 in Fig. 7, right side) discharges bursting spikes with an in-phase relationship, whereas antagonistic pairs (1 vs. 2 and 4 vs. 5 in Fig. 7, right side) exhibit anti-phase relationship with each other. These coordinated output patterns in an isolated brain preparation are comparable to the natural antennal movement.
The insect brain is composed of three distinct regions anteroposteriorly: the protocerebrum, deutocerebrum, and tritocerebrum. Sensory information received by the antennae is primarily conveyed to the deutocerebrum. Many anatomical studies clarified that the olfactory receptor afferents exclusively project to the primary olfactory center in the ventral deutocerebrum (antennal lobe), and non-olfactory (such as mechanosensory and gustatory) receptor afferents project to other regions from the deutocerebrum to the subesophageal ganglion (Fig. 8). In contrast to the olfactory pathway, the mechanosensory pathways have not been adequately described in any insect species. A recent anatomical study in P. americana described that mechanoreceptor afferents in the basal segments project to relatively dorsal area in the dorsal deutocerebrum (also known as the dorsal lobe), while mechanoreceptor afferents in the flagellum project to more ventroposterior areas in the dorsal lobe (Nishino et al. 2005). These antennal mechanosensory afferents also project up to the anterior region of the subesophageal ganglion. The central projections of the flagellar mechanosensory afferents exhibit a topographical pattern, reflecting their peripheral locations, in the deutocerebrum (Nishino et al. 2005).
It is generally accepted that the primary motor center for the insect antenna is located in the dorsal lobe. Although the antennal motor center has been little known in the cockroach, a recent anatomical study elucidated its organization (Baba and Comer 2008). At least 17 antennal motor neurons were found in the deutocerebrum, and they were classified into five types according to their morphology. Although the positions of cell bodies differ according to their type, the dendritic processes from these neurons are colocalized at the dorsal area of the dorsal lobe (Fig. 8). The dendritic zone is thought to be located just dorsally to the antennal mechanosensory center. On the other hand, the central morphology of two dorsal unpaired median (DUM) neurons has been elucidated: both the cell bodies are located at the dorsomedial region of the subesophageal ganglion, and bilaterally symmetrical axons from the cell bodies run down to both sides of antennal muscles.
Tactile information from the antennal mechanoreceptors may be relayed to the following neurons for further sensory processing and/or expression of appropriate behavior. In this context, it would be essential to study individual antennal mechanosensory interneurons, particularly in the animals with a simpler central nervous system. Thus far, several physiological studies have identified such interneurons in cockroaches. One of the best known interneurons in P. americana is the "giant" descending mechanosensory interneurons (DMIs) (Burdohan and Comer 1996). Of the two DMIs identified, one (DMIa-1) has its cell body in the protocerebrum, and the other (DMIb-1) has its cell body in the subesophageal ganglion (Fig. 9). The DMIa-1 axon extends fine branches into the ipsilateral dorsal deutocerebrum where the antennal mechanosensory and motor centers are thought to be located, runs to the contralateral hemisphere of the brain, and descends down to the abdominal ganglia while extending fine processes into the thoracic ganglia. The DMIb-1 axon also descends down in a similar morphological pattern. The DMIa-1 responds exclusively to the mechanical stimuli to the antenna, whereas the DMIb-1 is responsive to the stimuli to the head and mouthparts as well. The DMIs may be responsible for the control of an evasive locomotor behavior (see “Evasive behavior”).
Anemotaxis, a locomotor response to the wind, is thought to be a fundamental strategy to find odor sources located upwind. In three cockroach species (Blattella germanica, Periplaneta americana, and Blaberus craniifer), the anemotactic behavior in the absence of olfactory cues exhibited different patterns depending on both the species and wind velocity (Bell and Kramer 1979). B. craniifer directed and ran upwind in a wide range of wind velocities, while B. germanica oriented downwind. P. americana oriented upwind in low-wind velocities, while oriented downwind in high-wind velocities. When both the scape-pedicel and pedicel-flagellar joints of B. craniifer were fixed to prevent movement at the pedicel, positive anemotaxis was considerably impaired. This implies that the putative mechanoreceptors adjacent to the pedicel are crucial to detect wind direction and velocity.
The insect antenna has been considered to be rather non-responsive to the escape behavior. However, the responsiveness seems to be dependent on the tactile feature of the stimulants. For instance, if a cockroach (P. americana) comes in contact with a potential predator (spider), as sensed by the antenna, it would immediately turn away and escape from the spider (Comer et al. 1994). Similarly, cockroaches may discriminate tactile features (probably texture) between the spider and the cockroach by means of antennal probing (antennation) (Comer et al. 2003). The mechanoreceptors in the flagellum and the antennal basal segments are thought to be essential for acquiring tactile information and initiating escape response, respectively.
Since cockroaches exhibit a positive thigmotaxis, they tend to walk or run along the wall. During such wall-following, both the antennae extend forward to remain in contact with the adjacent wall. A behavioral study revealed that P. americana is capable of turning at 25 Hz during a rapid wall-following (Camhi and Johnson 1999). This high-frequency turn helps avoid collisions while maintaining body at an appropriate distance from the wall. Tactile cues regarding what part of the flagellum is in contact with the wall or is bended by the wall may be essential for such a high-performance wall-following behavior.
When an antenna of a searching cockroach (P. americana) contacts with a stable object in an open space, the animal may stop and approach toward the object with antennation (see the movie below). This behavior can be observed even in blinded animals, indicating that visual cues are unnecessary. Similarly, a tethered cockroach mounted on a treadmill may attempt to approach a stable object presented to the antenna (Okada and Toh 2000). This object-guided tactile orientation behavior is probably due to the thigmotactic nature of cockroaches (see "Wall-following"). Because the extent of turn angle depends on the horizontal position of the presented object, cockroaches can discriminate the position of objects by antennation. Removal of hairs in the scapal hair plates resulted in significant deterioration in the performance of tactile orientation, suggesting that the proprioceptors in the antennal joints are vital for the detection of an object’s position (Okada and Toh 2000).
Electrostatic field detection
It has recently been reported that cockroaches appear to avoid artificially generated electrostatic field (Hunt et al. 2005). This evasive response may help them avoid, for instance, friction-charged objects and high-voltage power lines. Newland et al. (2008) recently proposed a possible unique mechanism for electrostatic field detection in P. americana. After the antennal joints between the head and scape were fixed, the treated animal could no longer avoid electrostatic field. They proposed the following working hypothesis. As a cockroach approaches a charged field, biased charge distribution would be produced between the antennae and the cockroach's body. The antennae are then passively deflected by the Coulomb force in the electrostatic field. Finally, the antennal deflection may be detected by the hair plates at the head-scape joint.
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