Localising Sounds in Space

1
Localising Sounds in Space

• MSc Neuroscience
• Prof. Jan Schnupp
• jan.schnupp_at_dpag.ox.ac.uk

2
Objectives of This Lecture

• Acoustic Cues to Sound Source Position
• Cues to Direction
• Interaural Level Cues
• Interaural Time Cues
• Spectral Cues
• Cues to Distance
• Encoding of Spatial Cues in the Brainstem
• Divisions of the Cochlear Nucleus
• Properties of the Superior Olivary Nuclei
• Representation of Auditory Space in Midbrain And
  Cortex
• The auditory space map in Superior Colliculus
• The role of Primary Auditory Cortex (A1)
• Where and What streams in auditory belt
  areas?
• Distributed, panoramic spike pattern codes?

3
Part 1 Acoustic Cues
4
Interaural Time Difference (ITD) Cues

• ITDs are powerful cues to sound source direction,
  but they are ambiguous (cones of confusion)

5
Interaural Level Cues (ILDs)
ILD at 700 Hz
ILD at 11000 Hz

• Unlike ITDs, ILDs are highly frequency dependent.
  At higher sound frequencies ILDs tend to become
  larger, more complex, and hence potentially more
  informative.

6
Binaural Cues in the Barn Owl

• Barn owls have highly asymmetric outer ears, with
  one ear pointing up, the other down.
  Consequently, at high frequencies, barn owl ILDs
  vary with elevation, rather than with azimuth
  (D). Consequently ITD and ILD cues together form
  a grid specifying azimuth and elevation
  respectively.

7
Spectral (Monaural) Cues
8
Spectral Cues in the Cat

• For frontal sound source positions, the cat outer
  ear produces a mid frequency (first) notch near
  10 kHz (A). The precise notch frequency varies
  systematically with both azimuth and elevation.
  Thus, the first notch iso-frequency contours for
  both ears together form a fairly regular grid
  across the cats frontal hemifield (B). From Rice
  et al. (1992).

9
Adapting to Changes in Spectral Cues

• Hofman et al. made human volunteers localize
  sounds in the dark, then introduced plastic molds
  to change the shape of the concha. This disrupted
  spectral cues and led to poor localization,
  particularly in elevation.
• Over a prolonged period of wearing the molds, (up
  to 3 weeks) localization accuracy improved.

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Part 2 Brainstem Processing
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Phase Locking

• Auditory Nerve Fibers are most likely to fire
  action potentials at the crest of the sound
  wave. This temporal bias known as phase
  locking.
• Phase locking is crucial to ITD processing, since
  it provides the necessary precise temporal
  information.
• Mammalian ANF cannot phase lock to frequencies
  faster than 3-4 kHz.

Evans (1975)
https//mustelid.physiol.ox.ac.uk/drupal/?qear/ph
ase_locking
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Preservation of Time Cues in AVCN

• Auditory Nerve Fibers connect to spherical and
  globular bushy cells in the antero-ventral
  cochlear nucleus (AVCN) via large, fast and
  secure synapses known as endbulbs of Held.
• Phase locking in bushy cells is even more precise
  than in the afferent nerve fibers.
• Bushy cells project to the superior olivary
  complex.

sphericalbushycell
endbulbof Held
VIII nervefiber
13
Extraction of Spectral Cues in DCN
Bushy
Multipolar (Stellate)
Pyramidal
Octopus

• Type IV neurons in the dorsal cochlear nucleus
  often have inhibitory frequency response areas
  with excitatory sidebands. This makes them
  sensitive to spectral notches like those seen
  in spectral localisation cues.

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Superior Olivary Nuclei Binaural Convergence

• Medial superior olive
• excitatory input
• from each side (EE)

• Lateral superior olive
• inhibitory input
• from the contralateral
• side (EI)

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Processing of Interaural Level Differences
Lateral superior olive
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Processing of Interaural Time Differences
Medial superior olive
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How Does the MSO Detect Interaural Time
Differences?
From contralateral AVCN

• Jeffress Delay Line and Coincidence Detector
  Model.
• MSO neurons are thought to fire maximally only if
  they receive simultaneous input from both ears.
• If the input from one or the other ear is delayed
  by some amount (e.g. because the afferent axons
  are longer or slower) then the MSO neuron will
  fire maximally only if an interaural delay in the
  arrival time at the ears exactly compensates for
  the transmission delay.
• In this way MSO neurons become tuned to
  characteristic interaural delays.
• The delay tuning must be extremely sharp ITDs of
  only 0.01-0.03 ms must be resolved to account for
  sound localisation performance.

From ipsilateral AVCN
https//mustelid.physiol.ox.ac.uk/drupal/?qtopics
/jeffress-model-animation
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The Calyx of Held

• MNTB relay neurons receive their input via very
  large calyx of Held synapses.
• These secure synapses would not be needed if the
  MNTB only fed into ILD pathway in the LSO.
• MNTB also provides precisely timed inhibition to
  MSO.

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Inhibition in the MSO
From Brandt et al., Nature 2002

• For many MSO neurons best ITD neurons are outside
  the physiological range.
• The code for ITD set up in the MSO may be more
  like a rate code than a time code.
• Blocking glycinergic inhibition (from MNTB)
  reduces the amount of spike rate modulation seen
  over physiological ITD ranges.

20
The Superior Olivary Nuclei a Summary
Excitatory Connection

• Most neurons in the LSO receive inhibitory input
  from the contralateral ear and excitatory input
  from the ipsilateral ear (IE). Consequently they
  are sensitive to ILDs, responding best to sounds
  that are louder in the ipsilateral ear.
• Neurons in the MSO receive direct excitatory
  input from both ears and fire strongly only when
  the inputs are temporally co-incident. This makes
  them sensitive to ITDs.

Inhibitory Connection
Midline
IC
IC
MNTB
LSO
MSO
CN
CN
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Part 3 Midbrain and Cortex
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The Auditory Space Map in the Superior
Colliculus

• The SC is involved in directing orienting
  reflexes and gaze shifts.
• Acoustically responsive neurons in rostral SC
  tend to be tuned to frontal sound source
  directions, while caudal SC neurons prefer
  contralateral directions.
• Similarly, lateral SC neurons prefer low, medial
  neurons prefer high sound source elevations.

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Eye Position Effects in Monkey

• Sparks Physiol Rev 1986

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Possible Explanations for Sparks Data

• Underlying spatial receptive fields might shift
  left or right with changes in gaze direction, or
  hey might shift up or down.

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Creating Virtual Acoustic Space (VAS)
Probe Microphones
26
VAS response fields of CNS neurons
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Passive Eye Displacement Effects in Superior
Colliculus

• Zella, Brugge Schnupp Nat Neurosci 2001
• SC auditory receptive fields mapped with virtual
  acoustic space in barbiturate anaesthetized cat.
• RF mapping repeated after eye was displaced by
  pulling on the eye with a suture running through
  the sclera.

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Lesion Studies Suggest Important Role for A1
Jenkins Merzenich, J. Neurophysiol, 1984
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A1 Virtual Acoustic Space (VAS) Receptive Fields
C
B
A
19-255, EO, CF12, A2.19, D0.80, L0.50, 15 dB
54-94, EE, CF9, A2.77, D2.29, L0.19, 25 dB
51-02, EE, CF5, A7.92, D2.39, L0.14, 15 dB
D
E
F
Spikes per presentation
51-19, EO, CF17, A4.36, D1.49, L0.37, 20 dB
38-78, EO, CF7, A5.06, D2.59 L0.10, 35 dB
51-07, OE, CF5, A8.23, D2.84, L0.03, 35 dB
I
G
H
54-12, EI, CF8, A8.28, D2.39, L0.13, 20 dB
 
54-304, EE, CF28, A1.37, D1.77, L0.29, 15 dB
 
51-15, EE, CF21, A1.97, D3.03, L0.21, 20
dB  
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Predicting Space from Spectrum
Left and Right Ear Frequency-Time Response Fields
a
Virtual Acoustic Space Stimuli
d
Frequency kHz
Elev deg
e
b
c
f
Schnupp et al Nature 2001
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Examples of Predicted and Observed Spatial
Receptive Fields
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Higher Order Cortical Areas

• In the macaque, primary auditory cortex(A1) is
  surrounded by rostral (R), lateral (L),
  caudo-medial (CM) and medial belt areas.
• L can be further subdivided into anterior, medial
  and caudal subfields (AL, ML, CL)

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Are there What and Where Streams in Auditory
Cortex?
AnterolateralBelt

• Some reports suggest that anterior cortical belt
  areas may more selective for sound identity and
  less for sound source location, while caudal belt
  areas are more location specific.
• It has been hypothesized that these may be the
  starting positions for a ventral what stream
  heading for inferotemporal cortex and a dorsal
  where stream which heads for postero-parietal
  cortex.

CaudolateralBelt
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A Panoramic Code for Auditory Space?

• Middlebrooks et al.found neural spike patterns
  to vary systematically with sound source
  direction in a number cortical areas of the cat
  (AES, A1, A2, PAF).
• Artificial neural networks can be trained to
  estimate sound source azimuth from the neural
  spike pattern.
• Spike trains in PAF carry more spatial
  information than other areas, but in principle
  spatial information is available in all auditory
  cortical areas tested so far.

35
Azimuth, Pitch and Timbre Sensitivity in Ferret
Auditory Cortex
Bizley, Walker, Silverman, King Schnupp - J
Neurosci 2009
36
Cortical Deactivation

• Deactivating some cortical areas (A1, PAF) by
  cooling impairs sound localization, but impairing
  others (AAF) does not.
• Lomber Malhorta J. Neurophys (2003)

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Summary

• A variety of acoustic cues give information
  relating to the direction and distance of a sound
  source.
• Virtually nothing is known about the neural
  processing of distance cues.
• The cues to direction include binaural cues and
  monaural spectral cues. These cues appear to be
  first encoded in the brainstem and then combined
  in midbrain and cortex.
• ITDs are encoded in the MSO, ILDs in the LSO.
• The Superior Colliculus is the only structure in
  the mammalian brain that contains a topographic
  map of auditory space.
• Lesion studies point to an important role of
  auditory cortex in many sound localisation
  behaviours.
• The spatial tuning of many A1 neurons is easily
  predicted from spectral tuning properties,
  suggesting that A1 represents spatial information
  only implicitly.
• Recent work suggests that caudal belt areas of
  auditory cortex may be specialized for aspects of
  spatial hearing. However, other researchers posit
  a distributed panoramic spike pattern code that
  operates across many cortical areas.

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For a Reading List

• See reading lists athttp//www.physiol.ox.ac.uk/
  jan/NeuroIIspatialHearing.htm
• And for demos and media see
• http//auditoryneuroscience.com/spatial_hearing