The Auditory Nervous System

Cortex Processing in The Superior Olivary Complex Cortex Advantages of Two Ears

MGB Medial Geniculate Body • Improved detection / increased loudness Excitatory Alan R. Palmer GABAergic IC Inferior Colliculus • Removing interference from echoes GlycinergicInteraural Level Differences • Improved detection of sounds in Medical Research Council Institute of Hearing Research DNLL Nuclei of the Lateral Lemniscus interfering backgrounds University Park LateralInteraural Lemniscus Time Differences Nottingham NG7 2RD, UK Cochlear Nucleus • Spatial localization DCN • Detection of auditory motion PVCN MSO Lateral Superior Olive AVCN Medial Superior Olive Cochlea MNTB Medial Nucleus of the Trapezoid Body Superior Olive

Binaural cues for Localising Sounds in Space

20 dB

time 700 μs Interaural Time Differences (ITDs) Interaural Level Differences (ILDs)

Nordlund

Binaural Mechanisms of Sound Localization Binaural Hearing • 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 • Interaural level differences at high frequency are initially The ability to extract specific forms of auditory analysed in the LSO by input that is inhibitory from one information using two ears , that would not be ((ghigh fre quenc y) ear and excitatory from the other. possible using one ear only.

1 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 Caspary and Finlayson (1991) Irvine (1986)

Excitatory Inhibitory Interaural time differences ((qy)low frequency)

_ + + + +

Ipsilateral Contralateral The discharges of cochlear nerve fibres to lowlow--

100 100 frequency sounds are not random; they occur at particular times (phase locking). el (dB SPL) el (dB v Sound le

20 20 0.12532 0.125 32 Frequency (kHz) Caird and Klinke 1983 Evans (1975)

2 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 Response

0 Interaural Time Difference

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 Pena et al 2001

The coincidence detection model of Jeffress (1948) is the widely accepted model for lowlow--frequencyfrequency sound Matches between the inputs from the two ears localisation in the Barn Owl Nucleus Laminaris

Department of Neurophysiology,University of Wisconsin ALT TAB Fischer and Pena 2009

Pathways for analysing interaural time differences Ipsilateral Response To inferior colliculus Excitatory 0 Interaural Time Difference

Cochlear Cochlear Left Ear + Nucleus Nucleus Right Ear

Semicircular Canals + + +

Window MSO

Contralateral Large calyx synaptic ending

Barn Owl: Konishi et al 1988

3 0 μs Time Delay

0 μs -600 -300 0 300 600 ITD (μs)

Cochlear Cochlear Left Ear Nucleus Nucleus Right Ear

Se micir cul ar Canals

Window MSO

Auditory Nerve Activity Large calyx synaptic ending

0 μs Time Delay

Bekius et al 1999

Interaural Phase Sensitivity in the MSO Arrives at left ear 300 μs later than at the right Best Delay Noise

BF tones

300 μs

Cochlear Cochlear Left Ear Nucleus Nucleus Right Ear

Se micircular 1 ms 1 ms Canals

Guinea Pig Win dow Palmer et al., 1990 MSO

Cat Yin et al., 1986 Auditory Nerve Activity Large calyx synaptic ending

300 μs Time Delay

Coincident spikes

Yin and Chan (1988) Palmer et al 1990

Arrives at left ear 300 μs Smith et al 1993 0 μs Time Delay later than at the right Distribution of peaks of ITD functions in response to interaurally-delayed noise

300 μs Physiological range 0 μs

Cochlear Cochlear 80 Left Ear Nucleus Nucleus Right Ear

Semicircular Canals ones

r 60

Win dow MSO 40 Number of Neu of Number Auditory Nerve Activity 20 Large calyx synaptic ending

300 μs Time Delay 0 μs Time Delay 0 -500 0 500 1000 Interaural Delays (μs) Coincident spikes

McAlpine Jiang and Palmer 2001

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

80

60 urones

40 Number of Ne of Number 20

0 -500 0 500 1000 Interaural Delays (μs)

Grothe 2003 McAlpine, Jiang and Palmer 1996 McAlpine Jiang and Palmer 2001

1/8 1/4 1/2 cycle

600 0.5 Interaural PhaseDifference 1.0 s) μ 500 0.4 0.8 400 1/16 0.6 0.3 300 0.4 0.2

rmalised Response rmalised 200 ural Time Difference ( Difference Time ural o 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 Brand et al., 2002 McAlpine Jiang and Palmer 2001

325 Hz

ITD processing is BF-BF-dependent.dependent. 500 Hz ITD functions are steepest around midline.

700 Hz ed Response ed

-1000 -500 0 500 1000 The consequence of this is that: Normalis ITD (μs) 1.0 kHz

As ITD increases across the physiological range the activity at any frequency increases 1.4 kHz

-1000 -500 0 500 1000 -1000 -500 0 500 1000 McAlpine Jiang and Palmer 2001 Brand et al 2002 ITD (μs) ITD (μs)

5 Descending pathways

Spoendlin 1971

Spangler and Warr 1991 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

Warr 1978, Warr and Guinan 1979

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