Renata Filippini, PhD.
Post-doctoral researcher at the University of Arizona and University of Sao Paulo
The construction of an accurate spatial map is key for localization of sound sources not only for communication, but also for survival. Being able to figure out the characteristics of the environment allow us to interact with it in a safe and productive manner: as animals, for instance, such map would help us to identify danger, or food; as humans, communication is dependent on every sensory cue being correctly processed. That means, visual, acoustic and somatosensory maps have to be constructed independently, and then integrated as a whole.
Our brains produce acoustic maps based on analysis of the sounds that reach both ears in terms of differences in time, intensity and spectra (Middlebrooks and Green, 1991; Grothe et al., 2010). Such analysis takes place mostly in subcortical structures, by comparisons of signals carried by ipsi and contralateral pathways. Therefore, binaural hearing is indispensable to localization of sound sources, and the negative effect of hearing thresholds asymmetries between ears has been known for a while (Oddfield and Parker, 1986). Most of the acoustic map is believed to be analyzed at the level of inferior colliculus and medial geniculate body (Brainard, 1994), however, it is also long known that people with cortical lesions have a hard time to localize sounds presented on the hemifield contralateral to the damaged hemisphere (Sanchez-longo and Forster, 1957; Poirier et al., 1994), which means that cortical processing has an important role in this process.
What would, than, be the role of the Corpus Callosum (CC) in sound localization?
The CC, through numerous neuronal fibers, interconnects the cerebral hemispheres, thus participating in the integration of every sensory information that reaches the subject. In the visual modality, the CC has a very important role in image fusion at midline field (Lepore et al., 1986; Saint-Amour et al., 2004), but the extent to which the CC participate on sound localization, is not quite well understood. The CC fibers have been shown to be sensitive to interaural time differences, and it’s resection in cats resulted in less neurons responding to such cues at the auditory cortex (Lepore et al., 1997).
In the late 1980’s a few studies emerged focusing on sound localization in Split Brain patients. Split-brain patients are known like this because their CC is completely or partially absent – either as a consequence of congenital abnormalities (e.g., agenesis of the corpus callosum) or it has been surgically sectioned (e.g., callosotomy in cases of severe epilepsy) – thus the hemispheres do not exchange information with each other, and one could expect some hindering of the acoustic environment analysis such as localization.
In 1993, Poirier et al. investigated the responses of 4 complete acallosal patients (agenesis) to a sound localization task. The authors reported that those patients were still able to localize static and dynamic sounds, but they did so with much less accuracy than their matched normal controls. Because they were working with the hypothesis that the CC would have the same role in the auditory system as in visual regarding midfield fusion, the authors were surprised by the evidence that acallosal patients presented, just like controls, better performance for midfield sounds than for lateralized sounds. If the CC was responsible for the better performance in midline, how the acallosal subjects were responding in the same fashion?
The authors then suggested that the quasi-normal performance and the mid-line better performance were due to the reorganization of their auditory system, through re-routing of auditory fibers or increased use of ipsilateral pathways. In fact, with MRI and fMRI studies, today we do know that acallosal patients have larger anterior commissure (another interhemispheric pathway – Owen et al., 2013), which could account for some of the callossal functions in these patients.
The other hypothesis they had proposed – strengthening of ipsilateral pathways – was tested in a later study from the same research group. Lessard et al. (2002) tested the split-brain patients in a localization task, but this time they also presented the static and moving sounds in a monaural condition, i.e. with one ear occluded. For the binaural condition, the authors again observed quasi-normal performance for static sounds, with significantly worse performance for dynamic sounds. For the monaural condition, not surprisingly, normal subjects responded to sounds presented on the occluded ear hemifield as being presented on the middle line or on the functional ear hemifield. The surprise was that acallosal subjects had better performance than controls, presenting fewer mistakes when sounds were presented in the occluded ear hemifield. The authors suggested that this finding confirms the notion that in subjects with agenesis or early-callosotomized the reduced interaural comparisons that would happen through CC leads to a more efficient use of monaural cues.
Both of these studies observed responses of subjects that were born without the corpus callosum, therefore they would had more opportunities and time for neural reorganization. Hausmann et al. (2005), however, observed the responses of 2 late and 1 early-callosotomised patients. They observed that the late-callosotomized patients were also able to perform the localization task, but they had poorer performance as compared to both controls and early-callosotomised patient, indicating that the late-callosotomized had went to some normal development of the structures before surgery, and did not have the time to go through the reorganization of the system to perform in a quasi-normal manner as the early-callosotomised or the agenesis patients from the other studies.
Another finding from the Hausmann et al. study was that late-callosotomized patients presented a leftward bias, meaning that when sound was leading at the right ear (i.e. right hemifield, left hemisphere), they would hear it on middle line. The authors argued that the absence or reduction of the interhemispheric transfers might impact more the left hemisphere than the right hemisphere, and that this could be an evidence of hemispherical asymmetry for spatial recognition, with an advantage for the right hemisphere. Such asymmetry has been discussed for some time, and more recently image studies (Zundorf et al., 2014) have indeed observed that the right inferior parietal cortex may be more involved in processing central sound sources than the left.
In summary, these studies observed that split-brain patients maintain the ability to identify the sound source, but with decreased accuracy in comparison to neurologically normal subjects and even to a lesser degree when using dynamic stimuli. Such loss of accuracy is more evident in late-callosotomized patients than early ones, which might present a quasi-normal performance, probably due to the system plasticity. These differences in performance of split-brain patients compared to normal controls suggest that, even though most of sound source identification takes place on lower levels of the auditory system, the CC definitely participate, probably, refining the analysis, especially for dynamic and more complex sounds.
Interestingly, the more lateral a sound is presented, less accurate the performances are, showing that humans rely more on binaural cues as far from the central line the sound source is. And also, the leftward bias observed in one of those studies also speaks in favor of the left hemisphere being more dependent on interhemispheric analysis and bilateral cues than the right hemisphere. This would also explain the larger difficulties these patients have with moving sounds, once these dynamic sound analysis might rely more on the processing of information from both hemispheres.
Finally, the monaural data showing better performance for early callosotomized than for normal individuals, is a strong indication that the absence of comparisons between hemispheres promotes larger comparison between ipsi and contralateral cues, in lower levels of the auditory system.
Split-brain research has been extremely important for neuroscience in the last 50 years, yelding a Nobel Prize for Roger Sperry in 1981 for his findings regarding hemispheric specialization. Understandably, today these studies are not as popular, after all image techniques has been improving and advancing in anatomical and functional research in humans; and also, there are not as many split-brain subjects available to assess, since the corpus callosotomy is now seen as a last resource for the treatment of epilepsy. However, we should not forget the important role of such studies for science and medicine, and to understanding the role of the corpus callossum in sensory processing.
Renata Filippini is a post-doctoral researcher at the Neuroaudiology Lab from the Department of Speech Language, and Hearing of The University of Arizona. In 2012 she got her PhD in Rehabilitation Sciences from the University of Sao Paulo, Brazil, in which she studied the effects of auditory training in speech perception through the use of ABRs to complex sounds. Dr. Filippini’s current studies are focused on auditory temporal processing and auditory temporal masking, under supervision of Dr. Frank Musiek in US and Dr. Eliane Schochat in Brazil. She is funded by the Sao Paulo Research Foundation – FAPESP, Brazil.
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