1. Lecture 23 Giant neurons Locust hearing Omega Neuron Tonotopicity Cricket localization Owls

2. Neurons monitor and control: they encode transduced sensory input by firing rates; collectively in brains and ganglia they discriminate, integrate, initiate and coordinate behavioural outputs such as locomotion or signalling (stridulation). The gross structure of nerve cords, tracts, lobes, and ganglia gives a rough idea of the amount of information going to and from body regions. Brains are always at the head end. Metamerism may be evident in the layout of neurons: in segmented animals serial repetition of ganglia (e.g., in worms) is form that shows function: its serieal repetition relates to how the animal controls changes in segment girth and length during locomotion; other metameric neural examples are the sensory and motor nerve roots of a fish. The cross-sectional area of a giant axon attests to a premium on high-speed depolarization and is used to mediate escape. The shape of an omega neuron attests to a function in localizing sound sources. The neurosensory cells (chordotonal sensilla) of crista acustica show size gradations in association with frequency response.

3. Giant neurons were studied in the earliest days of neurophysiology. Giant neurons are widespread in animals, e.g., Annelids, Arthropods, Molluscs. They are adaptive in coordinating emergency escape: feather duster worms use giant neurons to withdraw into the safety of their tubes when attacked without ‘consulting’ the brain. These cells were used by early physiologists trying to understand depolarization of the nerve cell membrane. In 1936 J.Z. Young discovered that certain long structures present in squids (previously thought to be blood vessels) were actually single unusually large neurons. They had axons of unusually large diameter: up to 1 mm. A typical axon is about 40 microns in diameter: these giants are about 700 microns. They run through the length of the body..

4. Pictures taken from a website illustrating the dissecting out of a nervous preparation of the squid giant synapse (USCRC IBRO) Stellate ganglion in squid mantle. The stellate nerve contains a giant axon. This large-diametered motor nerve depolarizes very rapidly, ensuring nearly synchronous activation of mantle muscles in a jet-propelled escape. Varying thickness promotes different speeds of conductivity: longer are thicker and go faster so everything happens at once.

5. How does a locust discriminate sound frequencies? As with most ears, those of the locust are bilateral, a right and a left, each situated within a recess in the first abdominal segment. The plane of the tympanum is angled to face backward slightly. The auditory ganglion of each ear is visible through the transparent tympanum, its nerve running anteromedially to join the metathoracic ganglion. Also visible on and through the tympanum are dark brown chitinous structures (e.g., pyriform vesicle, folded body) that lie on top of the tympanum.

6. The tympanum (ear drum) is a very-much thinned region of the cuticle with a ganglion sitting more or less in the middle. Behind the tympanum, applied overtop of ganglion and acoustic nerve is a tracheal sac. Backing the membrane with air is an important adaptation: if the tympanum were backed by haemolymph of the circulatory system the tympanum’s movements would be significantly damped by the blood and it would not respond with sensitivity to the ariborne sound.

7. Old professor’s old lecture note At one time it was disputed whether insects could discriminate frequency (indeed it was disputed whether they had hearing capacity) [insect baloonists experiments]. But now we know better: the locust ear is a frequency discriminator. Müller’s organ analyses frequency by associating certain clusters of neurosensory cells with certain regions of the eardrum. For example, the pyriform vesicle is a tiny weight of cuticle within the eardrum associated with neurosensory transducing cells (d cells) located in the fusiform body.

8. Chordotonal sensilla occur in the ganglion, 60 to 80 in four groupings; each sensillum involves several cell types. The sensillum transduces the mechanical movements of the pyriform vesicle or other cuticular eardrum parts. When the modified dendritic region surrounded by the scolopale cell is mechanically stimulated (by sound and resulting eardrum movement) the axon develops an action potential and the neurosensory cell, by firings, sends information to the CNS. The cell’s position on the eardrum, its mechanical linkage, and the behaviour of the eardrum itself, codes for particular frequencies.

9. Fusiform body (fb) and pyriform vesicle (pv) and frequency discrimination. At 3-kHz sound input the whole ganglion follows the motion of the pyriform vesicle (pv); so both ends move in phase. But at the higher frequency of 10 kHz the relative motions of ganglion (K1) vs pv are quite different and the strand of nervous tissue (fb) is shaken and jolted, leading to many firings of the chordotonal neurosensory cells within. Stephen R.O., Bennet-Clark H.C. 1982. The anatomical and mechanical basis of stimulation and frequency analysis in the locust ear. J. exp. Biol. 99: 279-314. fusiform body pyriform vesicle

10. Scanning laser vibrometry used to investigate the movements of the eardrum when stimulated by different frequencies. James F.C. Windmill, Martin C. Gopfert and Daniel Robert 2004. Tympanal travelling waves in migratory locusts Journal of experimental Biology 208: 157- 168.

11. Travelling waves vs standing waves eardrum movement when subjected to four different frequencies; scanning laser videos show the complex movement of different regions; profiles: red is outward movement of the tympanum and green is inward movement Frequency analysis in the locust involves a “travelling wave that funnels mechanical energy to specific tympanal locations, where distinct mechanoreceptor neurones project”. “For each frequency the tympanal deflections do not stay in position, but travel across the tympanum from posterior to anterior... At 3.3 kHz the wave travels across the thin membrane, moving towards a focus point located at the folded body...”

12. Red is outward movement of tympanum green inward

14. Anatomical representation of frequency: tonotopicity: form and function As in ‘topographic’ – meaning ‘spatial organization’. Ear proper: 30-60 chordotonal sensilla in a linear array, the crista acustica. Organized tonotopically within the organ: proximal receptors tuned to low frequencies, more distal receptors tuned to higher frequencies. The form of the sensilla ‘tells’ one something about their function. KATYDID ANATOMY GENERATOR & EAR

15. Katydids and crickets have pressure difference ears Sound has access to both the front and back of the eardrum Katydids have 4 eardrums, two in each foretibia; the neurosensory cells line the trachea that runs between the eardrums.

16. Interneurons and shape specificity (From J. Insect Physiology, George Boyan, 1984) Interneurons that receive auditory input: note topographical similarity of omegas of cricket Gryllus and katydid Tettigonia, reflecting binaural comparison. Neurons can be identified across taxa based upon their morphology, e.g., making crossbody comparisons or as in the case of AN1 conveying activity from the prothoracic ganglion to the brain. efferent, afferent

17. Scientific American Huber & Thorson omega is in the prothoracic ganglion phase shifter Pressure difference ear with 4 different inputs

18. Adaptiveness of omega shape of the neuron of a cricket Omega interneuron: its name suggested by the shape, lies within the prothoracic ganglion of a cricket or katydid. It receives input from the acoustic nerve running back up the foreleg from the ears. Parts of a neuron: cell body (soma), dendritic arborization, axon. Omega neuron is here filled with green dye via the electrode that once monitored its firing activity; omega neurons occur in the prothoracic ganglion of a cricket as an overlain mirror- image pair; the firing of each feeds back upon and inhibits the activity of the other. Thus a slight difference in perception to one side is enhanced, supporting better localization. Gerry Pollack, Montreal Contralateral inhibition

19. SOUND LOCALIZATION: DETERMINING DIRECTION AND DISTANCE TO A SOUND SOURCE. How does a too-small female field cricket find her mate by phonotaxis using his too-long sound wave? We determine direction to sound sources by comparing IIDs: interaural intensity differences. These differences arise in a right and left ear because of different path lengths (one ear is closer to the sound than the other) and because of sound diffraction (bending) by the body. Small bodies relative to sound wavelength have minimal effect on diffraction. Large bodies make effective obstacles and create a ‘sound shadow’. Human ears are separated by ~21 cm. This distance is about the wavelength of a 800 Hz sound. For this wavelength the (diffraction) cast by the human head gives an intensity difference of about 8 dB. For higher frequencies, e.g., a tone of 10 kHz, this effect becomes more pronounced, e.g., a 20 dB drop in intensity at the farther ear for 10 kHz. Humans make use of IIDs, turning their head to equalize sound levels and so to face in the direction of the source of a sound. Assigned reading: Michelsen, A. 1998. The tuned cricket. New Physiol. Sci. 13: 32-38. Michelsen, A. & Lohe, G. 1995. Tuned directionality in cricket ears. Nature 375: 639- Michelsen A. et al. 1994. Physics of directional hearing in the cricket Gryllus bimaculatus J. comp. Physiol. A 175: 153-164.

20. Cricket directionality is achieved because the ears are pressure gradient ears, i.e., sound has access to both front and rear of the eardrum, and also because in crickets this back access involves cross-body transfer of sound in a large prothoracic transverse trachea. The activity of the eardrum is a resultant of pressure changes both outside and inside. And at any given orientation of the female cricket, the net pressure at each ear is governed by phase produced by path-length differences. The physiologists refer to IIDs: interaural intensity differences. The different path lengths to the rear of the eardrum create phase differences which activate right and left eardrums to differing extent. Phase changes with orientation. * Explain phase.

21. Because a cricket’s body is small relative to the song sound wavelengths it broadcasts, it cannot create useful interaural intensity differences IIDs by diffraction. Cricket call wavelength is about 70 mm; the distance between the leg-situated ears with the legs in walking position, is no more than 10 mm. The body as an obstacle causes no significant drop in intensity to a farther ear. The female cricket can turn 360º in relation to a distant calling male and IIDs remain nearly the same. Yet in fact female crickets localize male calls well, at night, at a distance and can readily walk toward that sound source. How do they do it?

22. Imagine sound from a male’s call reaching the front of the near eardrum. It also arrives at the inner surface of this same eardrum via 3 other routes : two prothoracic spiracles on the thorax (IS & CS: ipsilateral* spiracle and contralateral spiracle) and the contralateral tympanum. The path lengths of the three routes change as the female turns. Thus the sound pressures on the back of the eardrum will change with changing phase relative to those on the outside. So right and left eardrums show different activity as a function of body direction relative to the source. Sound reaching the back of the eardrum later than sound reaching the front is shifted in time, i.e., its phase has changed. *ipsilateral same side as source; contralateral opposite side *

23. Michelsen broadcast 4.5 kHz to female crickets in an arena, moving a speaker to 12 different surrounding positions and monitoring eardrum activity with a laser vibrometer. The dotted line P is a vector (magnitude and direction) for the driving force (pressure) at the eardrum for these 12 sound-source directions. The resulting directional pattern for the right ear is asymmetrical, i.e., as the phase angle changes there are side-to-side differences in eardrum activity which can be transduced and compared by the omega neurons of the prothoracic ganglion. Now the cricket has IIDs and a way of localizing the sound source in the absence of effective diffraction.

24. Important to the phase difference across the body is a strange disc-shaped structure within the transverse trachea – a block in the tracheal lumen that somehow increases the path distance for the sound – slows it down; this phase shifter changes the phase adaptively so that the cricket gets the best side-to-side differences for localization. The acoustic tracheal morphology is not the same in all crickets: it differs in a related group of small crickets which have two phase- shifters in parallel.

25. So what is the adaptive basis of pure-tone calling in crickets? Why does the cricket have to be tuned? Imagine it as it isn’t. What would be the workings of a cricket which produced a nonresonant song involving multiple frequencies? Gone would be the single simple sine wave whose timing relationships combine critically to make usable differences in perceived intensity between right and left ears. Superposed waves that became complex would vary inconsistently in right-left differences as a result of body orientation. The cricket needs a simple single sinusoid in order for the adaptiveness of phase to ‘express itself’. Cricket on the hearth is cheery for adaptive reasons. The voice of the last cricket Across the first frost Is one kind of goodbye It is so thin a splinter of singing. Carl Sandburg

26. Barn Owl: the ears of owls are asymmetrical for hunting by sound and their faces are sound collectors O.W.L Center Quiet flight so they don’t become an source of noise ; forward directed eyes for excellent depth perception;

27. Payne, R.S. 1971. Acoustic location of prey by barn owls (Tyto alba). J. exp. Biol. 54: 535-573. Birds aren’t ‘into’ external ears (pinnae) for aerodynamic reasons. The right and left ear openings of owls face forward and are hidden by head feathers that make the head and face look bilaterally symmetrical. But in some owl species, underneath the feathers, the two ear openings are dramatically asymmetrical. “One ear has its opening above the horizontal plane, the other below it” (Payne 1971). This is an adaptation for hunting prey (rodents) by listening in the dark to their incidental sounds as they scurry through dead leaves on the forest floor. “Eight parallel rows of feathers…form the heart-shaped periphery of the face. The opening of each ear lies at the focus of one-half of this heart, a curving wall of feathers which is almost, but not exactly, parabolic. The feathers in each curving wall are highly modified, having reduced vanes and rachises which, for their size are unusually thick…. They are also more densely packed than any other feathers on the owl’s body. If they are removed the array of holes formed by their empty sockets shows hexagonal ‘closest packing ‘[e.g., honey comb] indicating that they are as close together as physically possible….These adaptations suggest that there have been strong selective pressures favouring a curving wall that reflects sound – the usual sound-absorbent properties of feathers having been circumvented by emphasis of those surfaces which could act as reflectors, and orientation of them normal to incoming sound waves.”

28. Bilateral asymmetry in parabolic auditory sensitivity fields is an adaptation to capture prey using the prey’s incidental-movement sounds