Auditory Cortex (1)

Neurobiology of Hearing (Salamanca, 2012)

Auditory Cortex (1)

Prof. Xiaoqin Wang

Laboratory of Auditory Neurophysiology Department of Biomedical Engineering Johns Hopkins University

web1.johnshopkins.edu/xwang Outline

Lecture 1: Tonotopic organization and stimulus selectivity a) Anatomical structure of the mammalian auditory cortex b) Tonotopic organization of auditory cortex c) Firing patterns and tuning to preferred stimulus

Lecture 2: Temporal processing a) Coding of time-varying signals b) Temporal-to-rate transformation in A1 c) Temporal-to-rate transformation outside A1

Lecture 3: Spectral and intensity processing a) Spectral processing b) Intensity processing

Lecture 4: Spatial and auditory-feedback processing a) Spatial processing b) Auditory-feedback processing

1-1

The Notion of Tonotopic Organization in Auditory Cortex

1-2 What is unique about the auditory systems?

1) Longer subcortical pathway 2) Spectrally overlapping, time-varying input signal 3) Sounds entering the ear from anywhere at anytime 4) Hearing-speaking: sensory- motor processing

Left Ear Right Ear

1-3 More spiking synapses in subcortical nuclei

Visual Auditory

Graded transmission

spiking 1 spiking

1 3

1-4 Brodmann (1909) New World Monkey (Callithrix jacchus – common marmoset)

Auditory Old World Monkey cortex (Cercopithecus)

Human

Organization of auditory cortex is largely preserved across primate species

1-5 Overall organization of auditory cortex

Cat Imig and Reale (1980)

Primates Morel and Kaas (1992)

R C

C R 1-6 Tonotopic organization of auditory cortex: First demonstration in anesthetized cat (at Hopkins!)

C R

1-7 Woolsey and Walzl (1942) A1 P

C R

1-8 Woolsey and Walzl (1942) Is auditory cortex tonotopically organized?

1-9 Evans and Whitfield (1965) Lack of an orderly organization in unanesthetized cat

“Standard cortex”

Suprasylvian sulcus

A P

1-10 Goldstein et al. (1970), Neural Encoding Lab, BME, JHU Is there a columnar organization in auditory cortex?

1-11 Abeles and Goldstein (1970) How reliable are anatomical landmarks?

1-12 Merzenich et al. (1975) Auditory cortex is tonotopically organized

tonotopic axis

Suprasylvian sulcus

A P AES iso-frequency axis PES

1-13 Merzenich et al. (1975) Systematic changes of CF across auditory cortex

tonotopic axis

Slope = 1 oct/mm

A P

1-14 Merzenich et al. (1975) Tonotopical organization in marmoset auditory cortex

High frequency

Low frequency

High frequency

Low frequency

1-15 Bendor and Wang (2005) Tonotopic organization across mammals

1-16 Morel and Kaas (1992) “Why are Evans et al. and our single track penetrations so out of agreement with the orderly representation of the cochlea within AI reported by Merzenich et al.? First and foremost in our view is the different anesthetic state. There is no question that the sorts of anesthetics Merzenich et al. used render many cortical units unresponsive to sound. Further the effect is probably selective so that units with more indirect input pathways are more likely to be affected.” (p.190)

Goldstein and Abeles, Brain Res., 100:188-191 (1975)

1-17 What have we learnt from the old debate?

• Anesthetized Unanesthetized

• MGB input Cortical response

layer IV Other layers

• Multi-unit Single-unit

• Near threshold Supra-threshold stimulus

• Single hemisphere Averaging across hemispheres

1-18 “In this chapter and elsewhere, we have stressed the diversity of the neural coding properties of the units in the auditory cortex. This diversity makes the cortex a difficult region to study and makes it especially unattractive to those who like their science in neat packages. Let us hope that new studies, new techniques, and new findings will move us out of what will someday be called the early phases (or even the dark ages) of neuroscientific study of the cortex.”

Goldstein and Abeles, Handbook of Sensory Physiology, p.217 (1975)

1-19 Mysteries of Auditory Cortex

Why it’s so silent? Because of anesthesia &. non-optimal stimuli !

Onset responses to brief sounds Onset responses to continuous sounds (anesthetized rats) (anesthetized marmosets)

5 sec Tone!

DeWeese and Zador (2003)

1 sec deCharms and Merzenich (1996) 1-20 Auditory cortex is capable of sustained firing in awake animals

Primary Auditory Cortex Non-Primary Auditory Cortex (Stimulus: Tone) (Stimulus: Noise)

1-21 Wang et. al. (Nature, 2005) Auditory cortex neurons respond to preferred stimuli with sustained firing and adapt quickly to non-preferred stimuli

Primary Auditory Cortex Secondary Auditory Cortex

1-22 Wang et. al (Nature, 2005) What is the relationship between firing pattern and stimulus selectivity in auditory cortex?

Auditory cortex neurons respond to preferred stimuli with sustained firing and adapt quickly to non-preferred stimuli

1-23 From a stimulus’ point of view:

Responses to one particular sound by all neurons

Most Preferred

Stimulus preference Middlebrooks (2005)

Least preferred

“When a sound is heard, a particular population of auditory cortex neurons fire continuously throughout the duration of the sound. Responses of other, less optimally driven neurons fade away quickly after the onset of the sound.” (Wang et al. Nature 2005)

1-24 From a neuron’s point of view:

Responses of one neuron to entire acoustical parameter space

Acoustic parameter space

Preferred stimulus (sustained firing)

Non-preferred stimuli (onset firing)

Outside RF (no response)

1-25 Wang (Hearing Research, 2007) From a neuron’s point of view:

Responses of one neuron to entire acoustical parameter space

Acoustic parameter space

1-26 Wang (Hearing Research, 2007) Increased stimulus selectivity along ascending auditory pathway

Preferred stimulus (sustained firing) Auditory cortex Non-preferred stimuli (onset firing)

Thalamus

Inferior colliculus

Auditory nerve

1-27 Wang (Hearing Research, 2007) How responsive is auditory cortex during sleep? (unlike under anesthesia!)

1-28 Issa and Wang (2008) Auditory cortex is as responsive to sounds during sleep as during awake state

1-29 Issa and Wang (2008) However, SWS shows less excitation at low sound levels, …

1-30 Issa and Wang (J. Neurosci 2011) ..., and less inhibition at high sound levels

1-31 Issa and Wang (J. Neurosci 2011) SWS alters auditory processing across sound levels

1-32 Issa and Wang (J. Neurosci 2011) Summary of observations from auditory cortex in awake condition

1) Neurons in auditory cortex are high selective to acoustic stimuli. - Each neuron is only responsive to a small region of acoustic - As a result, each stimulus only excites a small number of neurons (“spatial sparseness”) 2) Neurons in auditory cortex are also highly responsive (fire plenty of spikes), but only to stimuli they like. - “spatial sparseness” does not result in sparse firing (i.e., transient responses) 3) “Selectivity” and “responsiveness” are closely coupled.

- Stimulus selectivity is a more useful measure than “sparseness” if you want to understand what a neuron actually does.

1-33 Suggested readings:

Tonotopic organization: 1. Woolsey CN and Walzl EM. Topical projection of nerve fibers from local regions of the cochlea to the cerebral cortex of the cat. Bulletin of the Johns Hopkins Hospital 71: 315-344, 1942. 2. Evans EF, Ross HF and Whitfield IC. The spatial distribution of unit characteristic frequency in the primary auditory cortex of the cat. J Physiol 179: 238-247., 1965. 3. Goldstein MH, Abeles M, Daly RL and McIntosh J. Functional architecture in cat primary auditory cortex: tonotopic organization. J Neurophysiol 33: 188-197., 1970. 4. Abeles M and Goldstein MH. Functional architecture in cat primary auditory cortex: columnar organization and organization according to depth. J Neurophysiol 33: 172-187., 1970. 5. Merzenich MM, Knight PL and Roth G. Representation of cochlea within primary auditory cortex in the cat. J Neurophysiol 38: 231-249, 1975. 6. Goldstein MH and Abeles M. Note on tonotopic organization of primary auditory cortex in the cat. Brain Res 100: 188-191., 1975. Firing pattern and stimulus selectivity: 7. Wang, X., T. Lu, R.K. Snider and L. Liang. Sustained firing in auditory cortex evoked by preferred stimuli. Nature 435: 341-346 (2005). 8. Wang, X. Neural coding strategies in auditory cortex. Hear Res. 229:81-93 (2007). 9. Issa, E. B. and X. Wang. Altered Neural Responses to Sounds in Primate Primary Auditory Cortex during Slow-Wave Sleep. J. Neurosci. 31:2965-2973 (2011)