The whisper and the siren
Dr Isabel Dean discusses how the brain codes the intensity of a sound
Think of the quietest sound that you can hear: a whisper, perhaps, or the sound of rustling leaves. Now think of the loudest sound that you can tolerate: a shout close to your ear, or an ambulance siren.
In listening to sounds that differ so greatly in loudness, you are performing a remarkable feat: in terms of sound volume, or ‘intensity’, those loud sounds are approximately a billion times more intense than the very quiet ones - and yet you can hear them all without trouble.
A long-standing mystery in hearing research is how the auditory system copes with receiving, and analysing, such a vast range of sound intensities.
One way in which auditory neurones respond to sound is by changing their level of electrical activity. Quiet sounds produce little electrical activity, or, more accurately, a low rate of ‘firing’ the brief electrical events that characterise all neurones; loud sounds cause auditory neurones to become more active, producing increased firing rates.
In this way, the firing rate of an auditory neurone provides a code for sound intensity: read out the firing rate, and you know the intensity of sound in the outside world.
The problem is that the range of sound intensities that produce an increase in neuronal firing rates seems far too narrow to cover the range of sound intensities that we encounter in everyday life. Most auditory neurones start to fire in response to very quiet sounds; their activity then increases rapidly as sound intensity increases, until they can raise their activity no further. This maximum point is typically reached by sounds that are only as loud as a normal conversation.
How, then, do neurones manage to code the shouting voice or the siren? My research, carried out in collaboration with other members of the UCL Ear Institute, has recently revealed a process that addresses this problem.
Although the firing rates of neurones change over only a narrow range of sound intensities, we have found that it is possible for neurones to alter the range of intensities to which they respond. Furthermore, these alterations in neuronal responses occur strictly according to the range of intensities that is currently present in the environment.
Our results suggest that, whilst you are sitting in a quiet room, your auditory neurones have adjusted their sensitivity so that they can increase their firing rates in response to very quiet sounds; however, if someone then turns up the radio, your neurones readjust their sensitivity to take account of the louder sound that now fills the room. Through experiments based on physiology and computational methods of neuroscience, we find that these dynamic changes in neuronal sensitivity adjust the code that is provided by the firing rates of auditory neurones, leading to greater accuracy of the code just around those sound intensities that are occurring most commonly.
In this way, the brain adapts to the intensities of sounds that are present in the listening environment. This adaptive response is rapid, taking place over the course of hundreds of milliseconds. An outstanding question is: how does the brain do this? What underlies these adaptations in auditory neuronal responses? It is this question that I am addressing in my current research.
In order to find out how adaptive coding of sound intensity is achieved, we first need to elucidate where in the auditory pathway the adaptation arises. The experiments that allowed us to first describe the adaptive effects focused on the brainstem, a part of the auditory pathway lying several stages beyond the inner ear, towards the highest centres in the brain. However, it is possible that the neuronal adaptation is initiated before this site, perhaps even at the so-called ‘primary’ auditory neurones that first carry information away from the inner ear itself.
Experiments that I have carried out this year through a collaboration with a research group at the Massachusetts Eye and Ear Infirmary, Boston, USA, have shown that this is indeed the case: the primary auditory neurones themselves display adaptation in their coding of sound intensity that is similar to that seen higher up the pathway, in the brainstem. These results give us clues as to what processes drive the adaptation, and where those processes originate.
I am also looking at the role of ‘feedback’ in the brain. When we hear, information is sent not only from our ears to our brains, but also back down the pathway, allowing our brains fine-control over responses to sound. It is possible that these feedback pathways are involved in the adaptation to sound intensity.We can test this possibility, by blocking the feedback - either pharmacologically, or by cooling the point in the brain from which the feedback pathways emanate, so as to inactivate them - and seeing whether the adaptation is altered.
Finally, I am starting to investigate how subthreshold neuronal electrical events - small events that either elicit or prevent firing activity - are affected during adaptation to sound intensity: for example, do the subthreshold events transmitted from one neurone to the next become stronger, do they change in frequency, or do neurones alter the way in which they respond to subthreshold events? I am addressing these questions through a combination of physiological experiments using extracellular techniques, which allow me to examine the firing activity of neurones, and patch-clamp techniques, which allow the measurement of the subthreshold electrical events occurring in auditory neurones.
This research addresses one of the great questions in brain research: that of how our brains respond to sensory information.
Our senses receive signals - sound, for example, or light - and our brains must respond to those signals, and interpret them, in order for us to be aware of the world around us. By revealing how auditory neurones adapt to the intensities of sound, the research gives insight into how we hear in the vast variety of listening environments that we encounter. Further, the results of these experiments might one day shed light on hearing disorders.
Lastly though, and perhaps most excitingly of all, discoveries that we make by studying hearing may reveal tools that the brain uses in common across other senses - thus advancing our understanding of how our brains inform us about the outside world.
Dr Isabel Dean spent her PhD studying the physiology and pharmacology of synaptic transmission in the in vitro cerebellum, in the Physiology Department at University College London. She then joined Prof David McAlpine's group at the UCL Ear Institute for a postdoctoral position, applying in vivo techniques to study functional aspects of neuronal adaptation in the auditory brainstem. In 2006, she took up a Royal Society Dorothy Hodgkin Research Fellowship at the UCL Ear Institute, through which she divides her time between her research into neural adaptation and working part-time on her family farm.
