In the previous posts, I have proposed that we should look at the ecological problem of sound localization, and that in terms of physiology we should go beyond tuning curves. However, if all of this is addressed, we still have a big problem. We are looking for “neural representations” or “codes”, but neural representations are observer-centric concepts that make little sense from the viewpoint of the organism, as I have discussed a few times before (for example there). Neural responses are not there to be read by some little homunculus, they are just neurons that are exciting other neurons, which you are not recording. Those other neurons are not “reading the code”, you are. Those neurons are just reacting instantly to the electrical stimulation of the neurons that constitute what we like to call “neural representation”.
Not everyone is receptive to the philosophical points, so let me just give one example. You could look at the reponses of lots of binaural neurons and realize they have lots of different tunings. So you could suggest: maybe sound location is represented by the most active neurons. But someone else realizes that the average response of all those neurons varies gradually with sound location, so maybe sound location is actually encoded in the average response? Wait a minute: why throw all this information away? maybe sound location is represented by the entire pattern of activity? The problem we are facing here is not that we don't know how to determine which one is true, but rather that all of these are true (the last one being trivially true). Yes, sound location is represented by the identity of most active neurons, the average response and the pattern of activity: there is a mapping between sound location and those different features. That is, you, the external observer, can look at those features and guess what the sound location was. What is this supposed to prove?
By focusing on neural representations, we are not looking at the right problem. What we want to know in the end is not so much how neural activity varies with various parameters of an experiment, but how neural activity constitutes the spatial percept, or perhaps more modestly, how it drives behavioral orientation responses. Now certainly looking at neural responses is a necessary first step, but we can't answer the interesting question if we stop there. So how can we answer the interesting question?
Well, I won't claim that I have a good answer because I think that's one of the major conceptual problems in systems neuroscience today. But one proposition that I think goes in the right direction is to do stimulations instead of, or in conjunction with recordings. Ideally, those stimulations should be such as to trigger behaviors. Is average activity the important feature? Stimulate neurons at different places and you should see the same orientation response. Is the identity of active neurons important? With the same experiment, you should see different responses, varying systematically with stimulated neurons.
It's possible: it has actually been done 45 years ago (Syka and Straschill, 1970). Electrical stimulation of the inferior colliculus with microelectrodes can trigger specific orienting responses. These days one could also probably do optogenetic stimulation. It's not going to be simple, but I think it's worth it.