Processing in The Superior Olivary Complex

Alan R. Palmer

Medical Research Council Institute of Hearing Research University Park Nottingham NG7 2RD, UK

Binaural cues for Localising Sounds in Space

time

Interaural Time Differences (ITDs) Interaural Level Differences (ILDs)

Binaural Mechanisms of Sound Localization

• Interaural time (or phase) difference at low frequency are initially analysed in the MSO by coincidence detectors connected by a delay line system.

• Interaural level differences at high frequency are initially analysed in the LSO by input that is inhibitory from one ear and excitatory from the other.

1 The Auditory Nervous System

Cortex Cortex

MGB Medial Geniculate Body

Excitatory GABAergic IC Inferior Colliculus GlycinergicInteraural Level Differences

DNLL Nuclei of the Lateral Lemniscus

LateralInteraural Lemniscus Time Differences Cochlear Nucleus DCN

PVCN MSO Lateral Superior Olive AVCN Medial Superior Olive Cochlea MNTB Medial Nucleus of the Trapezoid Body Superior Olive

Binaural Hearing

The ability to extract specific forms of auditory information using two ears, that would not be possible using one ear only.

2 Advantages of Two Ears

• Improved detection / increased loudness • Removing interference from echoes • Improved detection of sounds in interfering backgrounds • Spatial localization • Detection of auditory motion

20 dB

700 μs

Nordlund

Interaural level differences ((ghigh fre quenc y)

3 PARALLEL PROCESSING OF INFORMATION IN THE COCHLEAR NUCLEUS

To medial superior olive: information about sound To inferior colliculus: information about pinna localisation using timing (and possibly time coding of speech) sound transformations

To lateral superior olive: information about sound localisation using interaural intensity

To medial nucleus of the trapezoid body: information Either commisural or to inferior colliculus about sound localisation using interaural intensity information about sound level and voice pitch

To inferior colliculus: information about complex sounds (possibly place coding of speech)

Input from cochlear nerve

Interaural Level Difference Pathway

Excitatory Inhibitory

_ + + + +

4 Ipsilateral Contralateral

100 100 el (dB SPL) el (dB v Sound le

20 20 0.12532 0.125 32 Frequency (kHz) Caird and Klinke 1983

5 Caspary and Finlayson (1991) Irvine (1986)

Interaural time differences ((qy)low frequency)

The discharges of cochlear nerve fibres to lowlow-- frequency sounds are not random; they occur at particular times (phase locking).

Evans (1975)

6 PARALLEL PROCESSING OF INFORMATION IN THE COCHLEAR NUCLEUS

To medial superior olive: information about sound To inferior colliculus: information about pinna localisation using timing (and possibly time coding of speech) sound transformations

To lateral superior olive: information about sound localisation using interaural intensity

To medial nucleus of the trapezoid body: information Either commisural or to inferior colliculus about sound localisation using interaural intensity information about sound level and voice pitch

To inferior colliculus: information about complex sounds (possibly place coding of speech)

Input from cochlear nerve

Interaural Time Difference Pathway

The coincidence detection model of Jeffress (1948) is the widely accepted model for lowlow--frequencyfrequency sound localisation Response

0 Interaural Time Difference

7 Response

0 Interaural Time Difference

Department of Neurophysiology,University of Wisconsin ALT TAB

Ipsilateral

Contralateral

Barn Owl: Konishi et al 1988

8 Pena et al 2001

Matches between the inputs from the two ears in the Barn Owl Nucleus Laminaris

Fischer and Pena 2009

Pathways for analysing interaural time differences

To inferior colliculus Excitatory

Cochlear Cochlear Left Ear + Nucleus Nucleus Right Ear

Semicircular Canals + + +

Window MSO

Large calyx synaptic ending

9 0 μs Time Delay

0 μs

Cochlear Cochlear Left Ear Nucleus Nucleus Right Ear

Semicircular Can als

Window MSO

Auditory Nerve Activity Large calyx synaptic ending

0 μs Time Delay

Arrives at left ear 300 μs later than at the right

300 μs

Cochlear Cochlear Left Ear Nucleus Nucleus Right Ear

Se micir cul ar Canals

Window MSO

Auditory Nerve Activity Large calyx synaptic ending

300 μs Time Delay

Coincident spikes

Arrives at left ear 300 μs 0 μs Time Delay later than at the right

300 μs 0 μs

Cochlear Cochlear Left Ear Nucleus Nucleus Right Ear

Se micir cul ar Canals

Window MSO

Auditory Nerve Activity Large calyx synaptic ending

300 μs Time Delay 0 μs Time Delay

Coincident spikes

10 -600 -300 0 300 600 ITD (μs)

Interaural Phase Sensitivity in the MSO Best Delay

1 ms 1 ms

Yin and Chan (1988)

Smith et al 1993

11 Bekius et al 1999

Noise

BF tones

Guinea Pig Palmer et al., 1990

Cat Yin et al., 1986

Palmer et al 1990

Distribution of peaks of ITD functions in response to interaurally-delayed noise

Physiological range

80 ones

r 60

40 Number of Neu of Number 20

0 -500 0 500 1000 Interaural Delays (μs)

McAlpine Jiang and Palmer 2001

12 McAlpine, Jiang and Palmer 1996

1/8 1/4 1/2 cycle

1/16

McAlpine Jiang and Palmer 2001

Brand et al 2002

13 Grothe 2003

Brand et al., 2002

325 Hz

500 Hz

700 Hz ed Response ed

-1000 -500 0 500 1000 Normalis ITD (μs) 1.0 kHz

1.4 kHz

-1000 -500 0 500 1000 -1000 -500 0 500 1000 McAlpine Jiang and Palmer 2001 ITD (μs) ITD (μs)

14 Distribution of steepest slopes of ITD functions in response to interaurally-delayed noise Physiological range

80

60 urones

40 Number of Ne 20

0 -500 0 500 1000 Interaural Delays (μs)

McAlpine Jiang and Palmer 2001

600 0.5 Difference Phase Interaural 1.0 s) μ 500 0.4 0.8 400 0.6 0.3 300 0.4 0.2 200 ural Time Difference Difference ( ural Time ormalised Response a (cycles) N 0.2 0.1

Inter 100

0.0 -1000 -500 0 500 1000 0 0.0 Interaural Time Difference (μs) 0.00 0.25 0.50 0.75 1.00 1.25 1.50 Frequency (kHz)

McAlpine Jiang and Palmer 2001

ITD processing is BF-BF-dependent.dependent.

ITD functions are steepest around midline.

The consequence of this is that:

As ITD increases across the physiological range the activity at any frequency increases

15 Descending pathways

Spangler and Warr 1991

Warr 1978, Warr and Guinan 1979

16 Spoendlin 1971

Wiederhold and Kiang 1971

Function of the descending or centrifugal innervation

• Protection from acoustic trauma • Control of the mechanical state of the cochlea • Involvement in selective attention • Detection of complex signal in noise

17