Transcript Spatial Hearing

Localising Sounds in Space
MSc Neuroscience
Prof. Jan Schnupp
[email protected]
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?
Part 1: Acoustic Cues
Interaural Time Difference (ITD) Cues
ITD
ITDs are powerful cues to sound source direction,
but they are ambiguous (“cones of confusion”)
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.
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.
Spectral (Monaural) Cues
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 isofrequency contours for both ears
together form a fairly regular grid across
the cat’s frontal hemifield (B). From Rice
et al. (1992).
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.
Part 2: Brainstem Processing
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.
https://mustelid.physiol.ox.ac.uk/drupal/?q=ear/phase_locking
Evans (1975)
Preservation of Time Cues in
AVCN
spherical
bushy
cell
endbulb
of Held
VIII nerve
fiber
Auditory Nerve Fibers connect
to spherical and globular
bushy cells in the anteroventral 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.
Extraction of Spectral Cues in DCN
Bushy
Octopus
Multipolar
(Stellate)
Pyramidal
“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.
Superior Olivary
Nuclei: Binaural
Convergence
Medial superior olive
-excitatory input
from each side (EE)
Lateral superior olive
-inhibitory input
from the
contralateral
side (EI)
Processing of Interaural Level Differences
Sound on the
ipsilateral side
Lateral superior olive
I>C
Contralateral
side
C>I
Interaural intensity difference
Processing of Interaural Time Differences
Sound on the
ipsilateral side
Contralateral side
Medial superior olive
Interaural time difference
How Does the MSO Detect Interaural Time
Differences?
From contralateral AVCN
From ipsilateral 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.
https://mustelid.physiol.ox.ac.uk/drupal/?q=topics/jeffress-model-animation
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.
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.
The Superior Olivary Nuclei – a Summary
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.
Excitatory Connection
Inhibitory Connection
Midline
IC
LSO
IC
MNTB
MSO
CN
CN
Part 3: Midbrain and Cortex
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.
Eye Position Effects in Monkey
Sparks Physiol Rev 1986
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.
Creating Virtual Acoustic Space (VAS)
Probe Microphones
VAS response fields of CNS neurons
C15
Elev [deg]
90
90
1.3
45
0.9
00
0.4
-45
-90
-90
-180
-180 -135 -90
0
-45
00
45
90
180
90 135 180
Azim [deg]
0019/vas4@30
Microelectrode
Recordings
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.
Lesion Studies Suggest Important Role
for A1
Jenkins & Merzenich, J. Neurophysiol, 1984
A1 Virtual Acoustic Space (VAS) Receptive Fields
B
#19-255, EO, CF=12, A=2.19, D=0.80, L=0.50, 15 dB
D
C
#54-94, EE, CF=9, A=2.77, D=2.29, L=0.19, 25 dB
E
#51-19, EO, CF=17, A=4.36, D=1.49, L=0.37, 20 dB
G
#38-78, EO, CF=7, A=5.06, D=2.59 L=0.10, 35 dB
H
#54-12, EI, CF=8, A=8.28, D=2.39, L=0.13, 20 dB
#51-02, EE, CF=5, A=7.92, D=2.39, L=0.14, 15 dB
F
#51-07, OE, CF=5, A=8.23, D=2.84, L=0.03, 35 dB
I
#54-304, EE, CF=28, A=1.37, D=1.77, L=0.29, 15 dB
#51-15, EE, CF=21, A=1.97, D=3.03, L=0.21, 20 dB
Spikes per presentation
A
a
Left and Right Ear
Frequency-Time Response
Fields
Virtual Acoustic
Space Stimuli
16
4
Frequency [kHz]
Predicting Space from Spectrum
1
d
Elev[deg]
[deg]
Elev
4
1
c
-5 0 5 10
dB
1
0
-60
-180 -120 -60
100
0
e
0.5
0
200 ms
60
rate (Hz)
response
b
C81
16
0
60 120 180
Azim [deg]
200
0
0
100
ms 200
f
Schnupp et al Nature 2001
Examples of Predicted and Observed Spatial Receptive Fields
“Higher Order” Cortical Areas
In the macaque, primary
auditory cortex(A1) is
surrounded by rostral
(R), lateral (L), caudomedial (CM) and medial
“belt areas”.
L can be further
subdivided into anterior,
medial and caudal
subfields (AL, ML, CL)
Are there “What” and “Where” Streams
in Auditory Cortex?
Anterolateral
Belt
Caudolateral
Belt
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 posteroparietal cortex.
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.
Azimuth, Pitch and Timbre Sensitivity in
Ferret Auditory Cortex
Bizley, Walker, Silverman, King & Schnupp - J Neurosci 2009
Cortical Deactivation
Deactivating some cortical areas (A1, PAF) by cooling impairs
sound localization, but impairing others (AAF) does not.
Lomber & Malhorta J. Neurophys (2003)
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.
For a Reading List
See reading lists at
http://www.physiol.ox.ac.uk/~jan/NeuroIIspatialHearing.htm
And for demos and media see
http://auditoryneuroscience.com/spatial_hearing