Dendritic organization of sensory input to cortical neurons in vivo

Jia, H., Rochefort, N., Chen, X., & Konnerth, A. (2010). Dendritic organization of sensory input to cortical neurons in vivo Nature, 464 (7293), 1307-1312 DOI: 10.1038/nature08947

Consider a a cortical neuron in V1, layer 2/3, whose output shows sharp orientation tuning. What are the orientation tunings of the most important inputs to that neuron? What is the spatial distribution of these inputs in the neuron’s dendritic tree?

Here’s three possibilities. (1) You might expect the neuron to collect inputs which are broadly tuned for that same orientation (the “weak-bias model”). (2) Or, you might expect that the neuron as a whole collects inputs with various tunings, but that each dendritic branches would tend to collect inputs with a certain orientation. (3) Or, neither of these could be the case; maybe the inputs just take all sorts of orientations, randomly distributed among the dendritic tree. Here a picture of these possibilities from the News and Views:

three possibilities

Jia, Rochefort, Chen, and Konnerth analyzed the orientation tuning of such neurons as well as the orientation tuning of the calcium dynamics within the neuron’s dendritic tree. Their results support the third option (inputs with heterogenous tuning, spatially mixed).

While hyperpolarizing the cell, they found “calcium hotspots” in the dendritic tree, that is, places where there was a noticeable, localized calcium signal in response to stimulation. They then analyzed the orientation tuning of these hotspots. Figure 3b shows three hotspots and their calcium response to various drifting gratings (oriented visual stimuli):

Fig 3b; three hotspots and their calcium response to different orientations

Figure 3c shows what the orientation tuning was for all of the hotspots in one neuron:

Fig. 3c; spatial distribution of orientation tuning of calcium hotspots in the dendritic tree

The main results are that the orientation tuning of the hotspots is heterogeneous (all sorts of different tunings are found), and that there is no discernible spatial pattern to where the differently tuned hotspots are located within the dendritic tree.

Furthermore, they compared the histogram of the orientation tuning of hotspots between sharply tuned neurons and broadly tuned neurons, and found that they were similar, supporting the hypothesis that whatever it is that makes some neurons have sharper orientation than others tuning in their output, the cause is something other than having sharper orientation tuning in their inputs. Fig. 4d (OSI stands for “orientation selectivity index”):

Here’s an excerpt from the Nature editor’s summary: “Whether…. tuning is already encoded in a neuron’s dendritic inputs or whether the neuron itself computes its selective response has been unclear….They discover that, while all neurons receive distributed input signals coding for multiple stimulus orientations, each neuron makes its own ‘decision’ as to the orientation preference of its firing output.”

Some cautionary notes: (A} the News and Views makes it sound as if this study established linear dendritic summation. As far as I can tell, the study didn’t test that directly. (B) above, I said that possiblity 3 is that the inputs are “randomly distributed”; in the study, however, although the distribution SEEMED random, it’s possible that it is just organized in some complicated way that made it look random. (C) I could be wrong about this, but as far as I can tell, there’s no guarantee that the calcium hotspots are the “most important” synaptic inputs; they might be ones which just happen to have a high density of calcium channels (D) they are only looking in about four planes of focus and getting about 13 hotspots per neuron, so this is only a small proportion of all of the synapses (E) even if the set of strong synapses showed heterogeneous tuning, there could be many weak synapses that all have tuning that matches the output tuning. (F) I defined the hotspots as “noticeable, localized calcium signal in response to stimulation”, but this is pretty subjective. The article does not exactly specify an algorithm which was used to pick out the hotspots from within their imaging data. All the methods has to say about it is, “Transient changes in Ca2+ fluorescence (?f/f) were systematically examined by an adaptive algorithm, which involved small regions of interest (ROIs) of 3?×?4?µm, noise filtering and pattern matching.”

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5 thoughts on “Dendritic organization of sensory input to cortical neurons in vivo

  1. Thanks very much for the comment. Your interpretations are in fact very reasonable. The hotspots are indeed “noticeable, localized calcium signal in response to stimulation”. And in fact, I had to put high selection threshold to screen those hotspots out, because actually any part of dendrite that we recorded could be active at some time. Only by averaging over the stimulation time-window it became obvious to fish them out. However, as not being convincing that they are all what we call “signals”, they were simply ignored for this study. In a living brain, many things happen from time to time, I hope that in future studies I can distinguish more categories of signals. Of course, all depend on the quality of imaging data and level of analysis, which we are still working hard on at the moment. Yes, in the method section they were not described in detail, but we are preparing a protocol paper to completely illustrate them. What all appeared in this Nature paper were carefully written so not to mislead people. They stood well on solid ground, and I personally think that they are in line with a good philosophy. But don’t exaggerate them too much at the moment…

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  2. oops, sorry for a confusing point
    “…However, as not being convincing that they are all what we call “signals”, they were simply ignored for this study.”
    I mean, the non-hotspot area of dendrites were ignored because their activity could not be correlated with the visual stimuli that I presented to the mouse.

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  3. Thanks for your clarification!

    > What all appeared in this Nature paper were carefully written so not to mislead people. They stood well on solid ground, and I personally think that they are in line with a good philosophy. But don’t exaggerate them too much at the moment…

    I agree; I don’t think it was misleading. I didn’t mean “Some cautionary notes” to be critical — I don’t think I’ve ever seen an experiment which didn’t have caveats.

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