Spatial modulation of visual responses arises in cortex with active navigation

  1. E Mika Diamanti
  2. Charu Bai Reddy
  3. Sylvia Schröder
  4. Tomaso Muzzu
  5. Kenneth D Harris
  6. Aman B Saleem
  7. Matteo Carandini

  • Curated by eLife

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    Summary: This paper investigates the modulation of spatial signals in higher order visual areas in mice navigating virtual reality environments. Previous work demonstrated that the spatial position of an animal modulates neural activity in the primary visual cortex (V1). Here, the authors demonstrate that this spatial modulation however, is not a general feature of the visual circuit. Similar spatial modulation occurs in higher visual areas but not in lower visual areas, such as the lateral geniculate nucleus. Moreover, this work finds that spatial modulation was stronger when animals had more experience on the track and when the animals were actively performing a task, rather than when the animal was passively viewing the same virtual track. Since the first reports that visual neurons show modulation by spatial position during spatial navigation tasks, similar to that observed in hippocampal place cells, the source of this modulation has been an open question. This work adds new insight regarding this question, suggesting that it is likely either generated within the visual cortex itself or propagated in a top-down manner from higher brain areas, rather than in a bottom-up manner from the thalamus.

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Abstract

During navigation, the visual responses of neurons in mouse primary visual cortex (V1) are modulated by the animal’s spatial position. Here we show that this spatial modulation is similarly present across multiple higher visual areas but negligible in the main thalamic pathway into V1. Similar to hippocampus, spatial modulation in visual cortex strengthens with experience and with active behavior. Active navigation in a familiar environment, therefore, enhances the spatial modulation of visual signals starting in the cortex.

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  1. Version published to 10.7554/elife.63705 on eLife
  2. eLife

    Reviewer #2:

    This manuscript by Diamanti et al. describes their study on how visual neurons responded to identical visual stimuli at two different locations along a virtual linear track. Extending their previous result that spatial location modulates the neuronal activities in the primary visual cortex (V1), they now demonstrate that similar spatial modulation also occurred in the higher visual areas (HVAs), but not so much in a lower visual area, the lateral geniculate nucleus (LGN). In addition, they show that the modulation, measured by a spatial modulation index (SMI), was stronger when animals had more experience in the track and when the animals were actively performing a task rather than passively viewing the same virtual track. The authors have been responsive to comments by previous reviewers at a different journal. Data are appropriately analyzed and clearly presented.

    Since the finding that visual neurons are spatially modulated similarly as hippocampal place cells in spatial navigation tasks (Ji and Wilson, 2007; Haggerty and Ji, 2015; Fiser at al, 2016; Saleem at al, 2018), there has been increasing interest in identifying the source(s) of this modulation. This study adds new evidence to this puzzle, suggesting that it is more likely either generated within the visual cortex or top-down propagated from higher brain areas, rather than bottom-up propagated from the thalamus. This is an important contribution. However, there are concerns, mainly on the data interpretation and the clarification of the main conclusion, as elaborated below.

    1. Because experience and task engagement enhanced spatial modulation, the authors concluded in the abstract that "Active navigation in a familiar environment, therefore, determines spatial modulation...". This conclusion is too strong and not well-supported by the data. First, spatial modulation on Day 1, when the task was novel, was lower than on later days, but it was already much higher than 0 (Fig. 1h). Also the individual neuron data (Fig. 1e) display clear spatial modulation on Day 1. Therefore, "familiar environment" is not a requirement. Second, spatial modulation during passive viewing was much higher than 0 and was correlated with that during active navigation, as shown in Fig. 4e - Fig. 4l. Therefore, "active navigation" is not a requirement either. It is true that both active navigation and familiar environment enhanced spatial modulation. They did not "determine" spatial modulation.

    2. Related to the point above, the presence of spatial modulation in passive viewing reminds us that these cells in the visual system were still mainly driven by visual stimuli. The data in Fig. 4e,f are especially telling: the modulation in V1 was similar and highly correlated between active navigation and running replay. In addition, it is clear from all the raw traces in Fig. 1 and Fig. 2 that these cells did respond to the two segments with identical stimuli reliably with two peaks. The spatial modulation was just a change in one of the peaks. So the nature of the modulation is a "rate remapping" of the expected, classical visual responses. I believe, in order to maintain the big picture of what drives the activities of these neurons, it is beneficial to clarify that the "spatial modulation" is a modulation on top of the expected visual responses. This message is not explicitly conveyed in the current manuscript.

    3. The authors stated that spatial modulation is "largely absent in the main thalamic pathway into V1". This was based on the significantly weaker SMIs in LGN than those in V1 and HVAs. However, it is unclear whether the SMIs in LGN were still significant. The SMI values for both LGN buttons (Line #100) and LGN units (Line# 130) might be statistically significant from zero. The statistical comparison p-values should be given in both cases. Second, Figure 3 - figure supplement 1 b,f show that the SMI values in LGN could be predicted by spatial modulation, but not by visual stimuli alone or behavioral variations, just like those in V1 and HVAs. This seems to me good evidence for the presence of spatial modulation in LGN. Therefore, it is my opinion that the data do not support the complete lack of spatial modulation in LGN, but do clearly demonstrate weaker spatial modulation in LGN than in V1 and HVAs.

  3. eLife

    Reviewer #1:

    This paper investigates the modulation of spatial signals in higher order visual areas. A number of the findings are novel and interesting, including that signals in higher visual areas are not more influenced by spatial position that signals in V1, that this modulation is not a general feature of the entire visual circuit (i.e. LGN boutons in L4 of V1, as well as LGN units, show very little spatial modulation, and that spatial modulation decreases when mice are watching a replay of tunnel traversals. Overall, I think this paper provides new insight regarding position coding in visual systems. However, there are some points that should be addressed.

    1. The imaging data is from mice with different genetic backgrounds, as well as a mixture of gcamp6f and 6s. In addition, different reward protocols were used for different mice. Although the authors state in the methods that none of these factors impact their results, it would be good to include some quantifications to this effect (e.g. they could show the distribution of SMI for 6f data vs 6s data). While I don't expect the major observations to change if it turns out that some of these factors have as systematic effect, it could affect portions of the results where the dataset is split up - for example in the comparison between different higher visual areas, and the observation that spatial modulation appears to vary with receptive field location.

    2. The authors state that it is to be expected that LGN neurons respond more strongly in the first half of the corridor due to contrast adaption mechanisms. However, I did not see any quantification that could support this statement?

    3. When looking at the spatial modulation index, the authors switch between using median (e.g. Fig 1 and 2) and mean (Fig 4), t-test and rank-sum - and sometimes there is missing information regarding which (mean or median) they are reporting. The authors need to include more detail regarding these statistics.

    4. It was not clear to me if the authors are only imaging from layer 2/3 or if they also attempted to image deeper layers.

    5. Throughout the paper, the authors use 'firing rate' to refer to deconvolved calcium signal. Although this is stated in the methods, this wording can be misleading, especially since the paper also contains extracellular recordings of spiking activity.

    6. It was not clear to me how the dotted lines (e.g. Fig 1 b) were calculated.

  4. eLife

    Summary: This paper investigates the modulation of spatial signals in higher order visual areas in mice navigating virtual reality environments. Previous work demonstrated that the spatial position of an animal modulates neural activity in the primary visual cortex (V1). Here, the authors demonstrate that this spatial modulation however, is not a general feature of the visual circuit. Similar spatial modulation occurs in higher visual areas but not in lower visual areas, such as the lateral geniculate nucleus. Moreover, this work finds that spatial modulation was stronger when animals had more experience on the track and when the animals were actively performing a task, rather than when the animal was passively viewing the same virtual track. Since the first reports that visual neurons show modulation by spatial position during spatial navigation tasks, similar to that observed in hippocampal place cells, the source of this modulation has been an open question. This work adds new insight regarding this question, suggesting that it is likely either generated within the visual cortex itself or propagated in a top-down manner from higher brain areas, rather than in a bottom-up manner from the thalamus.

  5. Version published to 10.1101/832915 on bioRxiv