The distinct role of human PIT in attention control

Reviewer #1 (Public review):

The manuscript titled "The distinct role of human PIT in attention control" by Huang et al. investigates the role of the human posterior inferotemporal cortex (hPIT) in spatial attention. Using fMRI experiments and resting-state connectivity analyses, the authors present compelling evidence that hPIT is not merely an object-processing area, but also functions as an attentional priority map, integrating both top-down and bottom-up attentional processes. This challenges the traditional view that attentional control is localized primarily in frontoparietal networks.

The manuscript is strong and of high potential interest to the cognitive neuroscience community. Below, I raise questions and suggestions to help with the reliability, methodology, and interpretation of the findings.

(1) The authors argue that hPIT satisfies the criteria for a priority map, but a clearer justification would strengthen this claim. For example, how does hPIT meet all four widely recognized criteria, such as spatial selectivity, attentional modulation, feature invariance, and input integration, when compared to classical regions such as LIP or FEF? A more systematic summary of how hPIT meets these benchmarks would be helpful. Additionally, to what extent are the observed attentional modulations in hPIT independent of general task difficulty or behavioral performance?

(2) The authors report that hPIT modulation is invariant to stimulus category, but there appear to be subtle category-related effects in the data. Were the face, scene, and scrambled images matched not only in terms of luminance and spatial frequency, but also in terms of factors such as semantic familiarity and emotional salience? This may influence attentional engagement and bias interpretation.

(3) The result that attentional load modulates hPIT is important and adds depth to the main conclusions. However, some clarifications would help with the interpretation. For example, were there observable individual differences in the strength of attentional modulation? How consistent were these effects across participants?

(4) The resting-state data reveal strong connections between hPIT and both dorsal and ventral attention networks. However, the analysis is correlational. Are there any complementary insights from task-based functional connectivity or latency analyses that support a directional flow of information involving hPIT? In addition, do the authors interpret hPIT primarily as a convergence hub receiving input from both DAN and VAN, or as a potential control node capable of influencing activity in these networks? Also, were there any notable differences between hemispheres in either the connectivity patterns or attentional modulation?

(5) A few additional questions arise regarding the anatomical characteristics of hPIT: How consistent were its location and size across participants? Were there any cases where hPIT could not be reliably defined? Given the proximity of hPIT to FFA and LOp, how was overlap avoided in ROI definition? Were the functional boundaries confirmed using independent contrasts?

Reviewer #2 (Public review):

Summary

This study investigates the role of the human posterior inferotemporal cortex (hPIT) in attentional control, proposing that hPIT serves as an attentional priority map that integrates both top-down (endogenous) and bottom-up (exogenous) attentional processes. The authors conducted three types of fMRI experiments and collected resting-state data from 15 participants. In Experiment 1, using three different spatial attention tasks, they identified the hPIT region and demonstrated that this area is modulated by attention across tasks. In Experiment 2, by manipulating the presence or absence of visual stimuli, they showed that hPIT exhibits strong attentional modulation in both conditions, suggesting its involvement in both bottom-up and top-down attention. Experiment 3 examined the sensitivity of hPIT to stimulus features and attentional load, revealing that hPIT is insensitive to stimulus category but responsive to task load - further supporting its role as an attentional priority map. Finally, resting-state functional connectivity analyses showed that hPIT is connected to both dorsal and ventral attention networks, suggesting its potential role as a bridge between the two systems. These findings extend prior work on monkey PITd and provide new insights into the integration of endogenous and exogenous attention.

Strengths

(1) The study is innovative in its use of specially designed spatial attention tasks to localize and validate hPIT, and in exploring the region's role in integrating both endogenous and exogenous attention, as prior works focus primarily on its involvement in endogenous attention.

(2) The authors provided very comprehensive experiment designs with clear figures and detailed descriptions.

(3) A broad range of analyses was conducted to support the hypothesis that hPIT functions as an attentional priority map -- including experiments of attentional modulation under both top-down and bottom-up conditions, sensitivity to stimulus features and task load, and resting-state functional connectivity. These analyses showed consistent results.

(4) Multiple appropriate statistical analyses - including t-tests, ANOVAs, and post-hoc tests - were conducted, and the results are clearly reported.

Weaknesses

(1) The sample size is relatively small (n = 15), and inter-subject variability is big in Figures 5 and 6, as seen in the spread of individual data points and error bars. The analysis of attention-modulated voxel map intersections appears to be influenced by multiple outliers.

(2) The authors acknowledge important limitations, including the lack of exploration of feature-based attention and the temporal constraints inherent to fMRI.

(3) Prior research has established that regions such as the prefrontal cortex (PFC) and posterior parietal cortex (PPC) are involved in both endogenous and exogenous attention and have been proposed as attentional priority maps. It remains unclear what is uniquely contributed by hPIT, how it functionally interacts with these classical attentional hubs, and whether its role is complementary or redundant. The study would benefit from more direct comparisons with these regions.

(4) The functional connectivity analysis is only performed on resting-state data, and this approach does not capture context-dependent interactions. Task-based data analysis can provide stronger evidence.

(5) The study does not report whether attentional modulation in hPIT is consistent across the two hemispheres. A comparison of hemispheric effects could provide important insight into lateralization and inter-individual variability, especially given the bilateral localization of hPIT.

Author response:

Reviewer #1 (Public review):

The manuscript titled "The distinct role of human PIT in attention control" by Huang et al. investigates the role of the human posterior inferotemporal cortex (hPIT) in spatial attention. Using fMRI experiments and resting-state connectivity analyses, the authors present compelling evidence that hPIT is not merely an object-processing area, but also functions as an attentional priority map, integrating both top-down and bottom-up attentional processes. This challenges the traditional view that attentional control is localized primarily in frontoparietal networks.

The manuscript is strong and of high potential interest to the cognitive neuroscience community. Below, I raise questions and suggestions to help with the reliability, methodology, and interpretation of the findings.

Thank you for a nice summary of the key points of our study. Below you will find our responses to your questions.

(1) The authors argue that hPIT satisfies the criteria for a priority map, but a clearer justification would strengthen this claim. For example, how does hPIT meet all four widely recognized criteria, such as spatial selectivity, attentional modulation, feature invariance, and input integration, when compared to classical regions such as LIP or FEF? A more systematic summary of how hPIT meets these benchmarks would be helpful. Additionally, to what extent are the observed attentional modulations in hPIT independent of general task difficulty or behavioral performance?

Great suggestions! For the first suggestion, we will include a clearer justification in the revised manuscript. For the second one, all participants received task practice prior to scanning, and task accuracy exceeded 90% (we will explicitly report the accuracy rate in revision), suggesting the tasks were not overly demanding. Although ceiling effects limit the interpretability of behavioral-performance correlations, we argue that higher task demands would likely require greater attentional effort, leading to stronger modulation in hPIT, which aligns with our findings when we manipulated the attentional load.

(2) The authors report that hPIT modulation is invariant to stimulus category, but there appear to be subtle category-related effects in the data. Were the face, scene, and scrambled images matched not only in terms of luminance and spatial frequency, but also in terms of factors such as semantic familiarity and emotional salience? This may influence attentional engagement and bias interpretation.

The response of hPIT is generally insensitive to stimulus category, however, the reviewer is correct in noticing that attentional modulation in hPIT is slightly stronger to faces than scenes and scrambled images. Although faces used in the task had neutral expressions and the scene pictures were also neutral, it is indeed possible that potential semantic familiarity or emotional salience may contribute to the subtle category-related effects in the results of experiment 3. This point will be noted in the revised manuscript.

(3) The result that attentional load modulates hPIT is important and adds depth to the main conclusions. However, some clarifications would help with the interpretation. For example, were there observable individual differences in the strength of attentional modulation? How consistent were these effects across participants?

Yes, individual differences exist. In the revised manuscript, we will include individual subject data points in the figure 6B.

(4) The resting-state data reveal strong connections between hPIT and both dorsal and ventral attention networks. However, the analysis is correlational. Are there any complementary insights from task-based functional connectivity or latency analyses that support a directional flow of information involving hPIT? In addition, do the authors interpret hPIT primarily as a convergence hub receiving input from both DAN and VAN, or as a potential control node capable of influencing activity in these networks? Also, were there any notable differences between hemispheres in either the connectivity patterns or attentional modulation?

We agree that besides resting-state connection, task-based functional connectivity analyses would have the potential to provide additional information about whether hPIT serves as a convergence node or a control hub. While fMRI data are not the best to generate directional flow of information due to the low temporal resolution, we will conduct task-based functional connectivity analyses.

We also observed modest hemispheric asymmetries in connectivity—for instance, both left and right hPIT showed stronger connectivity with right-hemisphere attention nodes. This will be described in the revised supplement.

(5) A few additional questions arise regarding the anatomical characteristics of hPIT: How consistent were its location and size across participants? Were there any cases where hPIT could not be reliably defined? Given the proximity of hPIT to FFA and LOp, how was overlap avoided in ROI definition? Were the functional boundaries confirmed using independent contrasts?

The size and location of hPIT are generally consistent across subjects, as shown in Supplementary Figure 1. The consistency is also supported by figure 4C. The hPIT is defined by conjunction maps across three tasks and then manually delineated avoiding overlapping voxels with FFA and LOp. The FFA was defined using an independent contrast (Exp3 contrast [face-scene]) and the Lop location was defined by anatomical parcellation (Glasser et al., 2016).

Reviewer #2 (Public review):

Summary

This study investigates the role of the human posterior inferotemporal cortex (hPIT) in attentional control, proposing that hPIT serves as an attentional priority map that integrates both top-down (endogenous) and bottom-up (exogenous) attentional processes. The authors conducted three types of fMRI experiments and collected resting-state data from 15 participants. In Experiment 1, using three different spatial attention tasks, they identified the hPIT region and demonstrated that this area is modulated by attention across tasks. In Experiment 2, by manipulating the presence or absence of visual stimuli, they showed that hPIT exhibits strong attentional modulation in both conditions, suggesting its involvement in both bottom-up and top-down attention. Experiment 3 examined the sensitivity of hPIT to stimulus features and attentional load, revealing that hPIT is insensitive to stimulus category but responsive to task load - further supporting its role as an attentional priority map. Finally, resting-state functional connectivity analyses showed that hPIT is connected to both dorsal and ventral attention networks, suggesting its potential role as a bridge between the two systems. These findings extend prior work on monkey PITd and provide new insights into the integration of endogenous and exogenous attention.

Strengths

(1) The study is innovative in its use of specially designed spatial attention tasks to localize and validate hPIT, and in exploring the region's role in integrating both endogenous and exogenous attention, as prior works focus primarily on its involvement in endogenous attention.

(2) The authors provided very comprehensive experiment designs with clear figures and detailed descriptions.

(3) A broad range of analyses was conducted to support the hypothesis that hPIT functions as an attentional priority map -- including experiments of attentional modulation under both top-down and bottom-up conditions, sensitivity to stimulus features and task load, and resting-state functional connectivity. These analyses showed consistent results.

(4) Multiple appropriate statistical analyses - including t-tests, ANOVAs, and post-hoc tests - were conducted, and the results are clearly reported.

Thank you for a nice summary of the key points and strengths of our study.

Weaknesses

(1) The sample size is relatively small (n = 15), and inter-subject variability is big in Figures 5 and 6, as seen in the spread of individual data points and error bars. The analysis of attention-modulated voxel map intersections appears to be influenced by multiple outliers.

We agree that the sample size (n = 15) is not ideal, and we acknowledge that some data points in Figures 5 and 6 appear to be potential outliers. However, according to conventional outlier detection criteria, all data points are within three standard deviations of the group mean and were therefore retained for analysis. Moreover, the attention-modulated voxel intersection map shown in Figure 4C is insensitive to outliers, because the intersection map plotted is based on the number of subjects.

(2) The authors acknowledge important limitations, including the lack of exploration of feature-based attention and the temporal constraints inherent to fMRI.

Yes, we hope to address these limitations in future studies.

(3) Prior research has established that regions such as the prefrontal cortex (PFC) and posterior parietal cortex (PPC) are involved in both endogenous and exogenous attention and have been proposed as attentional priority maps. It remains unclear what is uniquely contributed by hPIT, how it functionally interacts with these classical attentional hubs, and whether its role is complementary or redundant. The study would benefit from more direct comparisons with these regions.

In this study, we define the ROI base on intersection across three different types of spatial attention tasks, and the hPIT stands out in showing spatial attentional modulation across tasks. This could be due to the weak lateralized responses in PFC/PPC. To evaluate whether a region qualifies as a priority map, we applied four criteria (as mentioned in introduction). While dorsal and ventral attention network (DAN and VAN) regions can be considered important components of the priority map system, our findings suggest that among the regions tested, hPIT meets all four criteria. In Experiment 2, we included regions such as VFC (as part of PFC) and IPS (as part of PPC), and our findings suggest these areas are more involved in top-down attention. We agree with the reviewer’s suggestion and will perform additional analysis on PPC and PFC.

(4) The functional connectivity analysis is only performed on resting-state data, and this approach does not capture context-dependent interactions. Task-based data analysis can provide stronger evidence.

We acknowledge that resting-state FC is limited in assessing task-specific communication. To further investigate the role of hPIT, we plan to conduct task-based functional connectivity analyses.

(5) The study does not report whether attentional modulation in hPIT is consistent across the two hemispheres. A comparison of hemispheric effects could provide important insight into lateralization and inter-individual variability, especially given the bilateral localization of hPIT.

We thank the reviewer for this suggestion. hPIT was localized bilaterally using the same intersection-based method in Experiment 1. We have now performed additional analysis and found in Experiment 3, the difference in attentional modulation between high and low load conditions was significant in the right hPIT but not in the left. This result will be reported in the revised manuscript.