Download Auditory Neuroscience - University of Sunderland

The Auditory System
(Lectures 7 and 8)
Harry R. Erwin, PhD
COMM2E
University of Sunderland
Background
• This is my speciality.
• I currently have three relevant grant proposals
active, in development or in review.
• I supervise research students in this area.
Organization of the Lecture
• Outside to inside.
• Issues associated with specific nuclei will be discussed.
• How the auditory system works will be addressed, to
the extent that it is currently known.
• The goal is to give you insight into how biologicallyinspired robots might hear.
• Perhaps you might want to build a system to localize
gunshots. Here’s an approach.
Resources
• Webster, Popper, and Fay, 1992, The Mammalian Auditory Pathway:
Neuroanatomy, Springer Handbook of Auditory Research, volume 1.
• Popper and Fay, 1992, The Mammalian Auditory Pathway: Neurophysiology,
Springer Handbook of Auditory Research, volume 2.
• Popper and Fay, 1995, Hearing by Bats, Springer Handbook of Auditory
Research, volume 5.
• Hawkins, McMullen, Popper and Fay, 1996, Auditory Computation, Springer
Handbook of Auditory Research, volume 6.
• Blauert, 1997, Spatial Hearing, revised edition, MIT Press.
• Nolte, 1993, The Human Brain, 3rd edition, Mosby Yearbook.
• Oertel, Fay, and Popper, 2002, Integrative Functions in the Mammalian Auditory
Pathway, Springer Handbook of Auditory Research, volume 15.
The auditory system is a typical
mammalian sensory system
• The auditory signal is processed by brainstem modules
before the information arrives at the cortex.
• Extensive cortical and somatic reafference is used to
tune the brainstem processing.
• Supports a series of functions:
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–
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–
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Reflexive movements (e.g., startle reflex)
Orientation towards stimuli (attention)
Localization (where is it?)
Classification (what is it?)
Multisensory integration (especially with vision and touch)
Illusions are a basic tool in
understanding sensory processing
• Illusions occur when the perceived stimulus does not
accurately reflect the actual stimulus.
• Usually reflect specific implementation in the sensory
processing.
• Examples of auditory illusions:
– The precedence effect
– Elevation illusions produced by filtered sounds
(based on the discussion in Middlebrooks, et al., in Oertel, Fay and
Popper, 2002)
The Precedence Effect
• You can usually localize clicks accurately in the horizontal
dimension. However, when the clicks are separated by a brief
delay, you experience an illusion.
• If the interval is < 5 milliseconds (msec), you experience a
single sound.
• If the interval is 1-5 msec, the perceived location is determined
by the leading click.
• If the interval is < 1 msec, the perceived location is intermediate
between the actual locations.
• Earlier and louder clicks influence the perceived location.
Elevation Illusions
• Your external ear (pinna) filters broadband sounds to
produce peaks and notches in the spectrum.
• These serve as cues to location, particularly in
elevation and resolving the front/back dimension.
• You can apply filters to a sound to confuse this
localization.
• The types of confusion that occur give insight into how
the cues are processed.
Implications
• The auditory system seems to have a minimum
resolution of 1-5 msec.
• There seems to be a trade-off between sound
intensity and timing.
• Different cues play different roles in
localization.
• Learning is probably important in calibrating
(and recalibrating) the auditory system.
Possible Localization Cues
• Azimuth (Jeffress, 1948)
– Interaural intensity difference
(IID)
– Interaural phase difference
– Interaural (onset) time
difference (ITD)
• Elevation
– Spectral shape
– Spectral notch movement
– Interaural line rotation
• Range
– Echo delay (biosonar)
– Target motion analysis
(TMA)
– Near-field stereophonic
audition (triangulation)
• Motion
– Doppler shift
– Phase shift
– Intensity shift
Components of the auditory system
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•
•
•
Neurotransmitters and receptors
Cell Types
Neural Circuits
Overall organization
Neurotransmitters
• Glutamate (Glu)
– AMPA receptors—excitatory, fast
– NMDA receptors—excitatory, learning, much slower
•
•
•
•
•
Aspartate—excitatory, fast, found in the cochlea.
GABA—standard inhibitory*, very slow.
Glycine—inhibitory*, fast, common in audition
Acetylcholine—excitatory
Various neuromodulators
*Remember the Cl- reversal potential!
Some basic cell types of the
auditory brainstem
•
•
•
•
•
Primary-like (PL)
Primary-like, notch (PL-N)
Phase-lock (onset)
Onset, lock (O-L)
Chopper
Primary-like (PL)
• Their output is similar to the output of auditory
neurons, hence the name. Only a few afferents,
resulting in some jitter.
• Low threshold current (LTC) K+ channels open quickly
and with a low threshold (10-15 mV depolarization
from resting).
• A second high threshold K+ current (HTC) then
activates at 20+ mV depolarization.
• These cells do not spike repetitively.
• Moderate time constant unless previously depolarized.
• Function as transducers
Primary-like, notch (PL-N)
• PL with many more afferents, which must sum
to threshold. The presence of the notch reflects
the very accurate initial spike timing and the
following refractory period. Very little jitter.
• Principle cells of the MNTB are PL-N because
they are tightly locked to their globular bushy
cells.
• Edge detectors
Phase-lock (Onset) and Onset, lock
(O-L) cells
• Octopus cells of the PVCN provide an initial well-timed
spike (like PL) cells, followed by a low level of activity.
However, they phase-lock to low frequency sounds (up to
800 Hz!, higher in some mammals and much higher in some
birds). Thick axons = short latencies.
• May function as pitch or coherence detectors.
• Sample many (>60) auditory neurons over a 200sec
integration window. LTC and IH (hyperpolarizationactivated) potassium channels. Extremely short membrane
time constant (~200sec) near their resting potential. Very
low input resistance, so they need lots of input to depolarise.
Chopper Cells
• Stellate cells that spike repetitively.
• Have a high-threshold potassium channel,
producing a classical Hodgkin-Huxley-like
cycle.
• As long as the depolarizing current is sustained,
will spike regularly.
Auditory Midbrain Rules of
Organization
• Many specialized nuclei, organized into parallel paths.
• Convergence at the inferior colliculus (IC), much of it inhibitory
or shunting. Left-to-right reversal at the IC (like vision). Does
the IC function like the basal ganglia? We may know in 3 yrs.
• Glycine (Gly) is the most common inhibitory neurotransmitter,
probably due to a faster time constant (~1 msec) than GABA
(~5 msec). Inhibitory rebound is extensively exploited to
produce delayed responses—a cell depolarizing enough to spike
after being hyperpolarized.
• Glutamate (Glu) is the usual excitatory neurotransmitter. AMPA
receptors are fast subtypes, so a time constant of 200 sec
(200x10-6 sec!) is typical. (Brand et al., 2002, in Nature indicate
100 sec for both Gly and Glu, which is probably too low.)
Duration Tuning Mechanisms
• Duration selective neurons seem to use inhibition and
inhibitory rebound.
• Involves inhibitory circuits. Can be modulated.
• Initially, a duration-selective neuron is inhibited from
firing in response to a sound.
• When the inhibition is released by the end of the
sound, the neuron depolarizes for a short interval.
• If delayed excitation arrives while the neuron is
depolarizes, it spikes. Otherwise it remains silent.
Break
Stages in Mammalian Audition
(Lecture 8)
•
•
•
•
•
•
External Ear (Pinnae)
Middle Ear
Inner Ear (Cochlea)
Inner Hair Cells
Type I Spiral Ganglion Cells
Cochlear Nucleus (dorsal CN
and ventral CN)
• Medial Nucleus of the
Trapezoidal Body
• Lateral Superior Olivary
Nucleus
• Medial Superior Olivary
Nucleus
• Lateral Lemniscus
• Central Nucleus of the
Inferior Colliculus
• Medial Geniculate Nucleus
• Auditory Cortex
The Principle Connections of the
Mammalian Auditory System
Planum
temporale
Planum
temporale
Corrected from
http://earlab.bu.edu/
intro/auditorypathways
.html
External Ears (Pinnae)
• Directional receivers, steerable in many mammals.
• The transfer function between the free-field sound
(with head not present) and the sound at the ear drum
is called the HRTF (head-related transfer function).
• Multipath interference occurs and seems to play a role
in generating elevation cues.
• Intensity, onset time, and phase differences between
the two ears seem to play a role in estimating azimuth
The Middle Ear
• Contains the stapes, incus, and
malleus.
• Translates the motion of the ear
drum into pressure waves in the
cochlea (inner ear).
• In the bat, muscles of the middle
ear contract or relax to mute the
sound of its cry and possibly to
normalize the intensity of the
echo based on distance to the
target.
• Figure from
http://oto.wustl.edu/cochlea/
intro1.htm
Inner Ear
• The cochlea (so called from the
snail-shell shape).
• A spiral organ with about 10004000 inner hair cells. The tip is lowfrequency.
• The strongest response to each
frequency is at a specific position,
producing a ‘tonotopic’ mapping
throughout the auditory system.
This is the only such mapping
known in mammals.
• Figure from http://hyperphysics.phyastr.gsu.edu/hbase/sound/ cochlea.html#c2
Inner Hair Cell
• Uses an excitatory neurotransmitter
(Glu or Asp)
• Vesicle release in response to
movement of stereocilia on the
apex. Logarithmic response to
pressure.
• Fast time constants. Bats can sense
time intervals less than 100 nsec,
probably by detecting interference.
• Figure from
http://www.neurophys.wisc.edu/www/aud
/johc.html
How the Inner Hair Cell Works
• Vesicle release appears to reflect Ca++ entry into the
cell (Ray Meddis). Motion of the stereocilia modulates
K+ influx, which causes Ca++ influx, but there is also
background Ca++ leakage, so vesicles are released even
without sound input. The release rate varies among
synaptic terminals, resulting in variation in sensitivity.
• The auditory neurons that synapse on the inner hair
cell use AMPA receptors and have a very short time
constant (~200 sec).
• The cochlea functions as a biological FFT.
Outer Hair Cells
• May adjust the motion of the
basilar membrane so that a specific
30 dB interval is chosen within the
120 dB range of sounds that can be
detected.
• An active cochlear amplifier is
likely but not fully proven.
• Would be controlled by reafference
from the superior olivary complex
(later).
• Figure from
http://www.neurophys.wisc.edu/www/aud
/johc.html
“Type I Spiral Ganglion Cells of the
Eighth Nerve”
• The auditory neurons (ANs), forming the “spiral
ganglion”.
• 10 to 70 synapse on each inner hair cell. Bipolar,
consisting of a dendritic element, a somatic
compartment, and a usually myelinated (nonmyelinated in humans, so slower) axonal element that
divides in the cochlear nucleus. Can synapse on
multiple inner hair cells. Excitatory (Glu). Extremely
sharp best frequencies.
• Cover a range of 30 dB in sensitivity.
• Show spontaneous activity (up to 140 Hz, Gulick).
How the Spiral Ganglion Cells
Work
• Multiple vesicles are often released at the inner hair
cell synapses, although one is enough to cause firing.
• Variable vesicle release rates by synapse seem to
produce the range of sensitivities seen. Vesicle release
reflects Ca++ entry into the cell. Integrate and fire
dynamics (Meddis), and spontaneous firing rates
reflect this. Some new results.
• Fast time constant ~200-300 µsec.
• Collectively can phase lock to a sinusoid up to 3-4
KHz (9 KHz in owls, Carr).
The Cochlear Nucleus (CN)
• The first stage of auditory processing after the cochlea.
• At the CN, the auditory neurons divide into two
branches, one dorsal and one ventral. Each branch may
terminate on multiple neurons.
• The cochlear nucleus is divided into the dorsal CN,
anterior ventral CN, and posterior ventral CN,
apparently with different functions. Attention plays a
role in the AVCN (Covey).
Dorsal Cochlear Nucleus (DCN)
• Laminar or layered structure. ‘Cerebellar-like’ per
Curtis Bell. Seems to play a role in estimating sound
elevation. Lesions have subtle effects.
• Somatosensory reafference is received from the
thalamic reticular nucleus (TRN), reporting on pinna
muscle activity. Issues here. Startle reflex.
• Glycinergic primary cells in the DCN appear to
respond to lines and notches centered on their best
frequencies, reporting to the IC.
• Complex inhibitory circuits in the DCN involving
sensory profiles produce this response.
DCN Circuits
• DCN cells participate in circuits that integrate
somatosensory data with sound.
• Also detect spectral notches in the signal with
moderate width.
• Output chopper, onset, and build-up patterns.
Ventral Cochlear Nucleus (VCN)
• Bushy cells (in the AVCN) are ‘primary-like’ cells that track the
spiking of auditory nerve cells directly. These have a dendritic
element, a soma, and a myelinated axon that passes to the
superior olivary complex, the lateral lemniscus, and to the
inferior colliculus, with excitatory signalling.
• Multipolar or stellate cells (in the DCN, AVCN, and PVCN)
project to the pontine tegmentum (SOC and LL). These are
‘chopper’ cells that periodically modulate the input signal.
• Octopus cells (PVCN) appear to be broadly tuned onset
detectors. Insensitive to intensity. Project to the pontine
tegmentum and then to the lateral lemniscus.
Superior Olivary Complex (SOC)
• Consists of the
– Lateral superior olivary nucleus (LSO)
– Medial superior olivary nucleus (MSO)
– Medial nucleus of the trapezoid body (MNTB)
• Size of the complex varies greatly among species as do
the sizes of the individual nuclei.
• In bats, cell counts of about 20000 (Ellen Covey,
personal communication)
• Secondary nuclei present as well.
• Plays a role in the stapedius reflex which protects the
middle ear from loud sounds.
Trapezoidal Body
• Large multipolar principal cells. Synaptic input is via
very large calyceal endings (end-bodies of Held). PL-N
dynamics.
• Input from globular bushy cells in the contralateral
AVCN.
• Reverses the sign of the signal. Inhibitory output.
• Projects to the ipsilateral LSO and LL. Glycinergic.
• High-frequency sensitive.
• Not considered important in humans.
Lateral Superior Olivary Nucleus
• Ipsilateral—excitatory, spherical bushy cells (PL)
• Contralateral—inhibitory input via the trapezoidal
body—globular bushy cells (PL-N)
• Outputs bilaterally to the lateral lemnisci and to the IC.
Glycine with glutamate or possibly aspartate. Mostly
chopper cells.
• Sensitive to high frequency sounds and used for
comparing the signal intensities at each ear.
• Small multipolar principal cells.
• Codes for auditory localization in azimuth.
Medial Superior Olivary Nucleus
• Excitatory input from both sides into separate
dendrites. Source: spherical bushy cells that track the
afferent signal.
• Feeds forward to the inferior colliculus, mostly
ipsilateral.
• Generates one or two spikes at sound onset. Other roles
possibly present.
• Important in large mammals with good low-frequency
hearing (sounds are diffracted, so intensity is not a
good cue for azimuth). Note that phase ambiguity
disappears over multiple frequencies.
Nucleus of the Central Acoustic
Tract
• Small, importance unknown
• Directly projects to SC and MGB, bypassing
IC.
• Large multipolar neurons
• Bilateral input from the AVCN
Lateral Lemniscus
• Major auditory tract. Contains 2nd, 3rd, and 4th order axons.
Seems to perform spectral analysis (e.g., vowel detection, line
spectra tracking) and detection of transients, and to have a role
in measuring the timing of echoes. (Like the Basal Ganglia…?)
• Octopus cell axons end in the ventral nucleus of the lateral
lemniscus (VNLL), with large calyceal endings. Part of the short
latency acoustic startle reflex pathway to the reticular formation.
Monaural. Transient detection.
• Stellate, bushy (excitatory) and MNTB, DCN (minor,
glycinergic) cells also project to the VNLL.
• VNLL is glycinergic. Choppers and PL. On-going research area.
• DNLL inputs binaural. Projects to the IC. Functional role
unknown.
Central Nucleus of the Inferior
Colliculus (Mesencephalon)
• Largest auditory structure of the brainstem on the roof of the
midbrain. A tectal structure behind the superior colliculus (SC).
There is a spatial mapping from the IC to the SC (that triggers
visual orientation to sounds in barn owl and possibly in
mammals).
• Primary point of convergence in the auditory brainstem. Sounds
arrive here 2-5 msec after the inner hair cells are activated.
• Bidirectional connectivity with the auditory cortex. Excitatory
inputs are received from the part of the AC (layer V) that then
receives the outputs. This is fast enough to support corticallycontrolled analysis of current sound afference.
IC components
• Small multipolar fusiform cells with tufted dendrites.
Cochleotopic = tonotopic laminar organization, uniting inputs
from all lower nuclei and the contralateral IC.
• The anterior portion of the laminae receive cortical inputs, while
the posterior portion receives brainstem and IC inputs.
• Stellate cells also present that cross the laminae.
• Recently it has been found that the signal at the IC is normalized
in intensity. Several possible mechanisms.
• Partly ‘cerebellar-like’ (Curtis Bell).
• Match/mismatch processing? Sparsification? Motion
processing?
• My current grant is in this area.
Medial Geniculate Nucleus (or
Body)
• AKA the auditory thalamus. Similar to the LGN (vision).
• Transduces the output of the colliculi for the auditory cortex.
Tonotopically organized. In bats, may encode distance.
• Ventral, dorsal, and medial (or magnocellular) divisions.
• Ventral division—about half the structure, projects to primary
auditory cortex (A1). Excitatory output.
• Dorsal division—projects to association auditory cortex (A2).
Auditory attention? Both excitatory and inhibitory output.
• Medial division—large multipolar neurons. Multisensory
arousal system? Both excitatory and inhibitory output.
Cerebellum
• Receives auditory data from the auditory cortex
and the pontine nucleus.
• Possible roles include coordinate
transformation, motor timing, and localization.
Primary Auditory Cortex (A1)
• Transverse gyri of Heschl
• True primary auditory cortex or koniocortex. Called
Area 41, A1, TC, or Kam/Kat depending on the author.
• Six-layered. Layer III functions differently from visual
cortex. Strong contralateral connectivity from III, V
and VI. Corticalfugal connectivity from V.
• Tonotopically organized with alternating bands
responding to a difference signal from the ears (+/-).
Sharp tuning and short latencies.
• Some visual sensitivity (from SC and late visual areas)
Secondary Auditory Cortex (A2)
• Parakoniocortex (Area 42, TB, or PB) in this area.
• Visual sensitivity.
• Multiple tonotopic maps, some complete. Longer
latencies, broader tuning, less sensitive to tones.
• In bats, the secondary tonotopic maps are quickly
sensitive to complex sounds.
• In mustached bat, there is a secondary area with a
bicoordinate frequency representation over a very
narrow frequency interval centered on the second
harmonic of the cry.
• Additional fields in bat are ‘delay tuned’.
Planum Temporale
• Smoother portion of the superior surface of the
temporal lobe (Area 22 or Tpt)
• Area 22 tends to extend somewhat onto the parietal
operculum and inferior parietal lobule in humans.
• On the left side, this is Wernicke’s area.
• Areas 39 and 40, the left inferior parietal lobule, is
probably a higher association area.
• Now suspected of being the point at which sounds are
correlated to auditory streams. Complex auditory
computation. Motion sensitivity? Visual sensitivity.
Other Language Cortices
• An association pathway (arcuate fasciculus)
connects Area 22, the inferior parietal lobule
(Areas 39 and 40, a complex multimodal
integration area), and the area triangularis of the
inferior frontal gyrus (Areas 44 and 45, Broca’s
area).
Where do things happen?
• Azimuth—binaural, measured in the SOC (MSO, LSO, and
MNTB).
• Elevation—monaural, probably based on DCN notch detection.
• Range, timing, and intervals—monaural, measured by the LL,
using inhibitory mechanisms.
• Line spectrum—monaural, measured by the LL.
• Sensory integration—for individual sounds, binaurally in the IC,
using evidence developed by lower nuclei.
• Comparisons between sounds—auditory cortex.
Reconstructing the acoustic scene
• How separate sound sources are distinguished, assigned to
sound streams, and localized is not understood.
• Attention probably chooses sounds out of background.
Otherwise, the first sound has preference. Ray Meddis thinks
sounds are disambiguated by ignoring ambiguous cues.
• Intervals between sounds are very important in disambiguating
them. Auditory neuroscientists are dubious about the ‘binding
problem.’
• Distinct sound characteristics are also important in assignment
to sound streams. Harmonics important as are spectral segments
of about 1 kHz.
• There are a number of interesting auditory illusions that we can
explore.
Some lessons to draw
• Dense representations are found throughout the auditory
brainstem. The sparse representations needed for associative
learning and retrieval seem to be cortical.
• The auditory brainstem has solved the problem of handling (and
modulating) duration tuning. This is currently a hard problem in
cortical modeling, probably because the role of inhibition and
inhibitory rebound is not well-understood. Recent results on
persistent activity are important.
• There is no evidence for a spatial map anywhere in the auditory
brainstem. This probably means space is represented in spectral
form. (Think spatial Fourier transform and Gabor functions.)
• Timing, not synchronization, probably solves the binding
problem in the auditory system.