Cortical Representation of Space in Deafness
 
 

The auditory system attributes a spatial location to all sounds we hear. This function is of substantial importance for speech understanding: two concurrent speech sounds can be significantly easier recognized if their sources are localized at different spatial positions (so-called squelch effect or binaural unmasking). In noisy environments, such as at a cocktail party, this effect is of cardinal importance for communication.


Is a congenitally deaf auditory system able to localize a sound source in space? This requires a sensitivity to interaural intensity differences of 1 dB and interaural time differences of 15-20 µs! Auditory localization ability is highly plastic and therefore potentially requires hearing experience for proper development.


The auditory cortex is an essential structure for spatial localization: functional inactivation of the auditory cortex eliminates the ability to localize sounds in space.


To investigate the cortical representation of auditory space, we first concentrated on the representation of the left and the right ear in the auditory cortex. We found that this organization is significantly affected by absence of hearing experience. Specifically, cortical processing of aural information was significantly reduced in congenital deafness, yielding high similarity of responses elicited by contralateral and ipsilateral stimulation. This is very different from hearing animals, where the cortex demonstrates specificity to contralateral ear in many functional measures. Additionally, a difference between cortical high-frequency and low-frequency representations have been found in hearing controls, absent in deaf cats. Finally, a complex spatio-temporal pattern of cortical activity („cortical propagating wave“) was for the first time observed with electrophysiological methods.  These waves were also affected by hearing experience. From these results follows that congenitally deaf subjects would significantly underestimate the azimuthal deviation of sound sources from midline locations. For details see Kral et al. (2009) and Tillein et al. (2010, 2011). Single-sided deafness affects the representation of space extensively, if its onset is early in life (see >>>).

 

Cortical organization of binaural cochlear implants in a hearing control. Left: Activation pattern observed 12 ms after a pulsatile stimulus with contralateral stimulation.  Cortical photograph shown in the middle. Right: Overlap of contralateral responses (height profile) and ipsilateral responses (color), indicating aural convergence in hearing controls (J Neurosci 2009).

binaural hearing with cochlear implants

Cortical propagating waves in a hearing control

(J Neurosci 2009). These cortical propagating waves were extensively modified in deafness.

ITD sensitivity is reduced in deafness

Cortical responses to stimuli with different interaural time differences (Y-axis). Shown is the firing rate per 1-ms bin in 16 synchronously recorded multiunits in hearing and deaf animals (Tillein et al., 2010, Cereb Cortex).

Sensitivity to interaural time difference was substantially reduced in cortical neurons of deaf animals (Tillein et al., 2010; Tillein et al., 2011), however, some rudimentary sensitivity (including so-called „peak ITD functions“) was found, too. This demonstrates that the network for coincidence detection in the superior olivary complex is essentially inborn. The decreased sensitivity to ITD demonstrates that hearing experience is required to maintain and refine the inborn patterns and develop full functionality in ITD detection.


Numerous additional deficits in cortical representation of ITD were found in the same study. This demonstrates the the interpretation of the extracted ITD cues by higher-order brain structures can not develop or degenerates in absence of hearing experience. Thus, to be able to localize sounds in space, the brain requires auditory experience (and possibly active interaction with acoustic space).


Particularly, a response that has been associated with suppression of reverberation and the so called „precedence effect“ was substantially reduced in deaf animals. This indicates that in congenital deafness, the network specialized in reverberation suppression does not develop properly.

ITD sensitivity functions: firing rate as a function of ITD within the first 15 ms post stimulus. Top: hearing animals, below: deaf animals. (Tillein et al., 2010, Cereb Cortex).

Units showing selectivity for ITD were found in both groups of animals, but a drop in sensitivity to ITD was observed in deaf animals, data from Tillein et al., 2010; figure from Kral & Sharma, 2012, TINS.