Neurobiology I: Cricket Song Production & Reception

All communication systems have three components. The transmitter sends a signal, which conveys information, to a receiver, which perceives the signal, processes it and responds to it. In crickets males are the transmitter and both males and females are the intended receivers. However, as we will see, other organisms can also perceive the signal and response to it.

Four types of cricket songs

• Males use the calling song to guide sexually receptive females to their burrow. Calling songs are species specific.

• Males use the courtship song to facilitate copulation after the female has entered the male’s territory.

• Following sperm transfer a male may sing a postcopulatory song. The function of this song is unclear, but it may be a form of postcopulatory mate-guarding behavior in which the male entices the female to remain close to him until egg fertilization starts.

• Males use the rivalry song in fights between neighboring territory holders or between territory holders and non-territorial “satellite males”.

Structure of cricket songs •  Pulse. The unitary sound normally produced by

a single movement of the sound producing apparatus.

•  Chirp. A sound which may consist of one or more pulses and which is normally heard by the human ear as a unitary event.

•  Trill. A sound in which the individual pulses run together to produce a more or less continuous note which may be amplitude-modulated.

•  Phase. One complete cycle of a song.

•  Amplitude modulation. A periodic change in the amplitude of the song or part of it. Moving from a chirp to a trill is often accompanied by a reduction in amplitude.

•  Frequency modulation. A periodic change in the frequency of the song or a part of it. Moving from a chirp to a trill is often accompanied by an increase in frequency.

Mechanics of song production •  Cricket songs are produced by a file and

scrapper system located on the forewings. The file is located along a vein on the undersurface of each forewing and consists of a series of ridges. The scrapper is a hardened area along the median edge of the opposite forewing. Sound is produced by rubbing the scrapper across the file as the wings are closed.

•  Vertically and horizontally oriented muscles in the thorax open the wings in preparation for sound production. Vertically oriented muscles close the wings and produce the song. Rubbing the scrapper across the file during wing closure produces a pure tone at approximately 5 kHz.

Neurophysiology of song production •  The cricket central nervous system is

a chain of 10 ganglia, 2 in the head, 3 in the thorax and 5 in the abdomen. Only the first two thoracic ganglia are necessary for singing in crickets.

•  Muscle contraction that controls the opening and closing of the wings is controlled by motor neurons with their cell bodies in the 2nd thoracic ganglion. These neurons fall into two synchronously firing groups that alternate with each other to open and close the wings. The alternate firing of antagonistic motor neurons is established by the powerful inhibition of one group during the discharge of the other group.

Neurophysiology of song production •  The sequential timing of the song

patterns is controlled by interneurons in the central nervous system and not by the motor neurons themselves. The cell bodies of these command interneurons, or pattern generators, are located in one of the cephalic ganglia and connect to other interneurons which in turn are connected to the motor neurons. Direct stimulation of the axon of command interneurons causes the song network to generate a perfectly normal calling-song pattern.

•  Excitation of the command interneuron is actively suppressed by the brain in the 10th instar cricket nymphs, or at other times when singing is inappropriate.

Genetics of song production •  Genetic crosses between closely

related species of crickets with different song characteristics produces offspring with songs of intermediate characteristics. These intermediate characteristics are encoded in the command interneurons.

•  An interesting aspect of these genetic crosses is that the intermediate characteristics of the songs depend on the species identity of the male and female used in the cross.

•  Genetic crosses suggest that many genes are required to specify the neuronal network responsible for song production.

Mechanics of song reception •  The acoustic organs of crickets are located on the fore

tibia. Each acoustic organ has two tympanal membranes, one facing forward and one facing backward. The posterior-facing tympanum is responsible for the transduction of acoustic stimuli.

•  Internal to the tympani are tracheal cavities crossed with thin tracheal membranes. The tympani transmit vibrational stimuli through the tracheal cavities to these membranes, which transmit the vibrations to the basement membrane.

•  Attached to the basement membrane is the crista acoustica containing 25-30 sense cells arranged longitudinally within the tibia. These sense cells are tuned to different sound frequencies between 3-17 kHz. The sense cells transmit acoustical signals to the CNS via the auditory nerve where the information is processed.

•  The acoustical organs in the tibia are connected to the prothoracic spiracles on either side of the body via the tracheal system. Pressure changes in the tracheal system that initiate at these spiracles influence the behavior of the tympani and the ability of a cricket to detect the direction of the acoustical signal.

Neurophysiology of sound reception

•  Acoustical organs in both male and female crickets are most sensitive to the dominant frequency of sound production. Sensitivity to the frequency of acoustical signals is represented by a frequency tuning curve. The acoustical organs of crickets are most sensitive to sound frequencies of 4-6 kHz, the same frequency produced by the sound production organ.

•  Crickets show a secondary sensitivity to sounds with frequencies between 40-80 kHz. These frequencies are produced by echo-locating insectivorous bats.

Genetics of sound reception

• Females that are hybrid offspring of two closely related species favor the intermediate songs of hybrid males over the songs of the pure songs of the parental species.

• Preference of hybrid females for the intermediate songs of hybrid males implies that the same genes control both the characteristics of song production and song reception.

Evolutionary convergence of hearing in a cricket parasitoid

•  Several species of tachinid flies in the tribe Ormiini are specialized parasitoids of singing crickets. Female parasitoids are attracted to the singing males crickets and deposit larvae on the bodies of the males or on the ground nearby. Larvae burrow into the mate cricket and consume it.

•  The acoustical organ of ormiine flies is located in the thorax and is similar in structure to the acoustical organ in crickets and very different from other non-ormiine tachinids.

•  The frequency tuning curve of female parasitoids is very similar to that of female crickets. Female parasitoids are most sensitive to frequencies in the 4-8 kHz range. Male parasitoids are much less sensitive to relatively low frequency sounds