Lecture 23
Giant neurons
Locust hearing
Omega Neuron
Tonotopicity
Cricket localization
Owls
• 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.
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.
•
.
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.
Pictures taken from a website
illustrating the dissecting out of
a nervous preparation of the
squid giant synapse (USCRC
IBRO)
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.
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.
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.
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.
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.
fusiform body
pyriform
vesicle
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.
James F.C. Windmill, Martin C. Gopfert and Daniel
Robert 2004. Tympanal travelling waves in migratory
locusts Journal of experimental Biology 208: 157168.
Scanning laser vibrometry used to investigate
the movements of the eardrum when
stimulated by different frequencies.
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...”
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
Red is outward movement of tympanum green inward
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
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.
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
Scientific American
Huber & Thorson
Pressure difference ear
with 4 different inputs
phase shifter
omega is in the
prothoracic
ganglion
Adaptiveness of omega shape of the
neuron of a cricket
Gerry Pollack, Montreal
Contralateral inhibition
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 mirrorimage 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.
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: 639Michelsen A. et al. 1994. Physics of directional hearing in the cricket Gryllus bimaculatus
J. comp. Physiol. A 175: 153-164.
*
Explain phase.
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.
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?
*
*ipsilateral same side as source;
contralateral opposite side
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.
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.
•
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 phaseshifters in parallel.
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
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;
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.”
Bilateral asymmetry in parabolic auditory sensitivity fields is an adaptation to
capture prey using the prey’s incidental-movement sounds