I’ve been in an email conversation with Paul Cisek, and in response to my confusion about what “representation” means do different people, he said this (and allowed me to post it here):
The business of “representations” is a bit of a semantic mess, because different people mean different things. Some just mean that neural activity correlates with something, which means we can decode it, and by that definition they obviously exist. However, by that definition, heartbeat represents running speed… so it’s a bit too inclusive. On the other extreme, some people believe that in order for any behavior function to take place, the external world must be internally “re-presented” inside the brain. However, this then raises the question of who looks at that representation (a homunculus?). You’ve probably heard all this before…
Anyway, my take on it is to think of representations along a continuum: At one end, we have simple feedback control circuits, in which internal states correlate with external stuff only insofar as being dynamically coupled to each other. I think a lot of neural activity is of this type, from the firing of cells in the stretch reflex to the firing of cells in the premotor cortex that guide the hand to a target. All of these representations are only understandable in the context of the circuit within which they reside, and the functional role of that whole circuit. For example, since premotor cell activity also varies with things like arousal, number of targets, target value, etc., you cannot really “decode” anything from them unless you know all of those variables (e.g. are running a highly controlled neuroscience experiment). I think the vast majority of neural activity is of this type – dynamical coupling that drives the system to a good state.
However, some neural activities are less modulated by internal states, and more “objectively” related to the outside world. For example, while cells in the insula might respond to an apple only when you’re hungry, because they play a pragmatic role in guiding feeding behavior, cells in IT cortex might respond to apples regardless of hunger or any other aspect of context. These are what I would call “descriptive” – in the sense that their functional role really is to convey information about the outside world. Frankly, I think such things are pretty rare in the brain. But the value of thinking about representations along such a continuum is that we can think of evolutionary scenarios in which a pragmatic representations, embedded within some control circuit, could have gradually become “divorced” from all of those contextual influences – for the simple reason that sometimes it’s good to have objective knowledge. For example, if I’m wondering around and see an apple when I’m not hungry, it’s useful to make a note in my cognitive map so that I can come back later when I am hungry. Again, these kinds of representations are probably a small subset of neural activity, but they probably do exist and have a phylogenetic history.