The Auditory System (Lectures 7 and 8)

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The Auditory System (Lectures 7 and 8)

• Harry R. Erwin, PhD
• COMM2E
• University of Sunderland

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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.

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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
  biologically-inspired robots might hear.
• Perhaps you might want to build a system to
  localize gunshots. Heres an approach.

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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.

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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
• 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)

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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)

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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 lt 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 lt 1 msec, the perceived
  location is intermediate between the actual
  locations.
• Earlier and louder clicks influence the perceived
  location.

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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.

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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.

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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

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Components of the auditory system

• Neurotransmitters and receptors
• Cell Types
• Neural Circuits
• Overall organization

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Neurotransmitters

• Glutamate (Glu)
• AMPA receptorsexcitatory, fast
• NMDA receptorsexcitatory, learning, much slower
• Aspartateexcitatory, fast, found in the cochlea.
• GABAstandard inhibitory, very slow.
• Glycineinhibitory, fast, common in audition
• Acetylcholineexcitatory
• Various neuromodulators
• Remember the Cl- reversal potential!

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Some basic cell types of the auditory brainstem

• Primary-like (PL)
• Primary-like, notch (PL-N)
• Phase-lock (onset)
• Onset, lock (O-L)
• Chopper

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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

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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

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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 (gt60) auditory neurons over a 200?sec
  integration window. LTC and IH (hyperpolarization-
  activated) 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.

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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.

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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 responsesa 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.)

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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.

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Break
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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

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The Principle Connections of the Mammalian
Auditory System
Planum temporale
Planum temporale
Corrected from http//earlab.bu.edu/
intro/auditorypathways.html
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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

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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

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Inner Ear

• The cochlea (so called from the snail-shell
  shape).
• A spiral organ with about 1000-4000 inner hair
  cells. The tip is low-frequency.
• 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.phy-astr.gsu.edu/h
  base/sound/ cochlea.htmlc2

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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

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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.

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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

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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
  (non-myelinated 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).

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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).

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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).

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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.

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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.

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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.

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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.

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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.

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Lateral Superior Olivary Nucleus

• Ipsilateralexcitatory, spherical bushy cells
  (PL)
• Contralateralinhibitory input via the
  trapezoidal bodyglobular 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.

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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.

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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

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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.

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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
  cortically-controlled analysis of current sound
  afference.

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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.

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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 divisionabout half the structure,
  projects to primary auditory cortex (A1).
  Excitatory output.
• Dorsal divisionprojects to association auditory
  cortex (A2). Auditory attention? Both excitatory
  and inhibitory output.
• Medial divisionlarge multipolar neurons.
  Multisensory arousal system? Both excitatory and
  inhibitory output.

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Cerebellum

• Receives auditory data from the auditory cortex
  and the pontine nucleus.
• Possible roles include coordinate transformation,
  motor timing, and localization.

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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)

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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.

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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 Wernickes 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.

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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,
  Brocas area).

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Where do things happen?

• Azimuthbinaural, measured in the SOC (MSO, LSO,
  and MNTB).
• Elevationmonaural, probably based on DCN notch
  detection.
• Range, timing, and intervalsmonaural, measured
  by the LL, using inhibitory mechanisms.
• Line spectrummonaural, measured by the LL.
• Sensory integrationfor individual sounds,
  binaurally in the IC, using evidence developed by
  lower nuclei.
• Comparisons between soundsauditory cortex.

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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.

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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.