Decades of neuroscientific research has sought to understand medial temporal lobe (MTL) involvement in perception. Apparent inconsistencies in the literature have led to competing interpretations of the available evidence; critically, findings from human participants with naturally occurring MTL damage appear to be inconsistent with findings from monkeys with surgical lesions. Here we leverage a 'stimulus-computable' proxy for the primate ventral visual stream (VVS), which enables us to formally evaluate perceptual demands across stimulus sets, experiments, and species. With this approach, we analyze a series of experiments administered to monkeys with surgical, bilateral damage to perirhinal cortex (PRC), a MTL structure implicated in visual object perception. Across experiments, PRC-lesioned subjects showed no impairment on perceptual tasks; this originally led us (Eldridge et al., 2018) to conclude that PRC is not involved in perception. Here we find that a 'VVS-like' model predicts both PRC-intact and -lesioned choice behaviors, suggesting that a linear readout of the VVS should be sufficient for performance on these tasks. Evaluating these data alongside findings from human experiments, we suggest that results from Eldridge et al., 2018 alone can not be used as evidence against PRC involvement in perception. These data suggest that the experimental findings from human and non-human primate literature are consistent, and apparent discrepancies between species was due to reliance on informal accounts of perceptual processing.
All scripts used for analysis and visualization can be accessed via github at https://github.com/tzler/eldridge_reanalysisAll stimuli and behavioral data used in these analyses can be downloaded via Dryad
Data from: Inconsistencies between human and macaque lesion data can be resolved with a stimulus-computable model of the ventral visual streamDryad Digital Repository, doi:10.5061/dryad.r4xgxd2h7.
- Tyler Bonnen
- Tyler Bonnen
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Animal experimentation: All experimental procedures conformed to the Institute of Medicine Guide for the Care and Use of Laboratory Animals and were performed under an Animal Study Protocol approved by the Animal Care and Use Committee of the National Institute of Mental Health, covered by project number: MH002032.
- Lila Davachi, Columbia University, United States
This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Genuinely new discovery transcends existing knowledge. Despite this, many analyses in systems neuroscience neglect to test new speculative hypotheses against benchmark empirical facts. Some of these analyses inadvertently use circular reasoning to present existing knowledge as new discovery. Here, I discuss that this problem can confound key results and estimate that it has affected more than three thousand studies in network neuroscience over the last decade. I suggest that future studies can reduce this problem by limiting the use of speculative evidence, integrating existing knowledge into benchmark models, and rigorously testing proposed discoveries against these models. I conclude with a summary of practical challenges and recommendations.
The synchronization of canonical fast sleep spindle activity (12.5–16 Hz, adult-like) precisely during the slow oscillation (0.5–1 Hz) up peak is considered an essential feature of adult non-rapid eye movement sleep. However, there is little knowledge on how this well-known coalescence between slow oscillations and sleep spindles develops. Leveraging individualized detection of single events, we first provide a detailed cross-sectional characterization of age-specific patterns of slow and fast sleep spindles, slow oscillations, and their coupling in children and adolescents aged 5–6, 8–11, and 14–18 years, and an adult sample of 20- to 26-year-olds. Critically, based on this, we then investigated how spindle and slow oscillation maturity substantiate age-related differences in their precise orchestration. While the predominant type of fast spindles was development-specific in that it was still nested in a frequency range below the canonical fast spindle range for the majority of children, the well-known slow oscillation-spindle coupling pattern was evident for sleep spindles in the adult-like canonical fast spindle range in all four age groups—but notably less precise in children. To corroborate these findings, we linked personalized measures of fast spindle maturity, which indicate the similarity between the prevailing development-specific and adult-like canonical fast spindles, and slow oscillation maturity, which reflects the extent to which slow oscillations show frontal dominance, with individual slow oscillation-spindle coupling patterns. Importantly, we found that fast spindle maturity was uniquely associated with enhanced slow oscillation-spindle coupling strength and temporal precision across the four age groups. Taken together, our results suggest that the increasing ability to generate adult-like canonical fast sleep spindles actuates precise slow oscillation-spindle coupling patterns from childhood through adolescence and into young adulthood.