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  1. Evaluation Summary:

    This study compares the roles of two interconnected dorsal pathway visual cortical areas, CIP and V3A, during perceptual decisions based on judging the tilt of 3D visual patterns. The potential impact of the paper stems from the novelty of directly comparing these two interconnected brain areas in perceptual decisions, and gives insight into their relative roles.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #3 agreed to share their name with the authors.)

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  2. Reviewer #3 (Public Review):

    This is a very extensive study (numbers of neurons recorded, tasks, thorough analyses). The paper is well written and the logic of the analyses is clearly explained. Only in some places, my impression was that some analyses might have been lengthy or redundant (for example, Figure 4). Several interesting new findings were: the presence of choice probabilities in V3A with a larger sample of neurons, the noise correlations, and in particular the analysis of the pre-saccadic activity and the comparison between V3A and CIP.

    One potential weakness of this study is that a large part of the results is entirely expected. We know for a long time that V3A provides the input to CIP (the Nakamura study used the term 'LIP' but covered CIP as well). Therefore, most findings in this study are what one would expect when comparing an earlier area to a higher area in the dorsal stream hierarchy (receptive fields, latencies, tolerance to distance, choice probabilities). On the other hand, there are not that many studies comparing two mid-level areas for which the connectivity is known. In the future, studies like this one will certainly contribute to building better models of the visual cortex in general and of the dorsal stream in particular.

    Another limitation of this study is the use of choice probabilities as such. As the authors themselves point out, the interpretation of CPs is difficult since they probably result from a combination of factors. Moreover, the discrepancy between the Elmore study and this study shows how easy it is to come to the wrong conclusions. It is noteworthy that the choice-related activity in V3A grows markedly 200-1000 ms after stimulus onset, but is absent in the first interval (in which the animals most likely decide on the stimulus), consistent with a feedback signal from higher areas if one wants to investigate the relation between neural activity and behavioral performance, it is far more powerful to use causal perturbation techniques. Finally, it is inherent in this type of follow-up study that a large part consists of the re-analysis of data previously acquired in CIP.

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  3. Reviewer #2 (Public Review):

    In this study, Doudlah et al test how neurons from two interconnected areas of the posterior parietal cortex respond during a task in which animals have to judge the tilt of a 3D stimulus and plan a saccade toward a direction related to their percept. This study is an extension of a study from the same group published in elife in 2020 (Chang et al. 2020). Here, they compare the results of this previous experiment, in which they recorded the activity of neurons from the Caudal IntraParietal area (area CIP), to new results acquired in cortical area V3a. The working hypothesis is that V3a represents low-level visual features while CIP integrates this information and transforms it into a decision signal related to the animals' choice. First, they show that both areas respond to the same task in a very similar manner. Neurons from both areas show strong selectivity to different features of the stimuli, including viewing distance, and 3D orientation. Interestingly, they show that CIP neurons encoded the 3D pose of the stimuli and animals' choice related to the orientation of these stimuli more strongly than V3a neurons. This suggests hierarchical processing of visual information, with feedforward transformation of sensory information into choice-related signals from V3a to CIP. In addition, they show that both areas show similar perisaccadic activity during a visually guided saccade.

    Strengths
    The hypothesis proposed by the authors is clear and well presented. Results clarify the role of V3a in the processing of depth by the visual cortex. It also shows that V3a's role probably extends the extraction of visual features.
    In general, data and analyses are clear and make sense altogether. Comparing how neurons from different areas are of high interest in order to understand how information is processed along the cortical hierarchy and allow them to put results from the parietal cortex in perspective with sensory processing in the visual cortex.

    Weakness
    I have few concerns about this article. My main concern is related to the analysis related to saccadic-related activity in V3a and CIP. Since monkeys perform a visually guided saccade, it is difficult to interpret neuronal activity during the saccade as perisaccadic. In this task, monkeys fixate for 1300 ms. Then, a target stimulus appears and they have to saccade toward it in less than 500 ms. They interpret variations of activity as perisaccadic. Such a task design does not allow us to dissociate between saccadic or visual responses. I am therefore not fully convinced by the last section of the analysis about the hierarchical processing of presaccadic activity.

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  4. Reviewer #1 (Public Review):

    This manuscript by Doudlah and colleagues is a comparison of CIP and V3a in monkeys during the performance of perceptual decisions about 3D visual stimuli. Monkeys performed a 3D visual tilt discrimination task in which they reported the tilt of a 3D stimulus by making a saccade to the correct saccade target corresponding to that direction of tilt. These two areas span the parietal-occipital junction and are both relatively infrequently studied compared to more commonly studied occipital and parietal visual and visuomotor cortical areas. The comparison is particularly novel as these areas have not been directly compared in past work during such decisions. A major strength of the study is the comparison of activity in these two brain areas recorded from the same animals performing the same task (2 of the 3 V3A monkeys were the same as the 2 CIP monkeys). The study gives novel insight into the relationship and relative hierarchical relationship between the two areas in visual feature processing and higher-order 3D spatial representations, with CIP showing higher-order spatial representations and more choice-correlated responses. Furthermore, the study finds a greater modulation of V3A activity by extraretinal factors, suggesting that V3A be characterized more as "association" than "visual cortex"

    Major findings of the study:

    1. 3D pose representations are more prominent in CIP than in V3A, but V3A shows that 3D orientation is more strongly and specifically encoded in V3A.

    2. Choice-correlated activity was stronger in CIP.

    3. Presaccadic activity was observed in both areas prior to the choice, with earlier onset in V3a. The CIP presaccadic activity is consistent with the temporal integration of presaccadic activity in V3a.

    Overall the study gives insight into the functioning and relationship between these dorsal stream areas and has the potential for high impact by virtue of explicating the roles of these less explored visual and parietal cortical areas in visual feature processing and saccadic choice.

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