Biology subjects

DiCarlo, J. J.

Publications and source records attributed to DiCarlo, J. J..

At least 19 recordsLinked to original sources

bioRxiv2024

The effects of object category training on the responses of macaque inferior temporal cortex are consistent with performance-optimizing updates within a visual hierarchy

How does the primate brain coordinate plasticity when learning to discriminate new objects? We measured consequences of object learning on macaque inferior temporal (IT) cortex, a key waypoint supporting object recognition in the ventral visual stream. Neural activity in task-trained monkeys IT showed increased object selectivity, enhanced linear separability across objects, and more object-invariant representations compared to task-naive monkeys. To model these differences, we developed a computational framework using anatomically-mapped artificial neural network (ANN) models of the ventral stream with various learning algorithms. Simulations revealed that gradient-based, performance-optimizing updates of ANN internal representations accurately approximated observed IT cortex changes. These models predict novel training-induced phenomena in IT cortex, including changes independent of object identity and ITs alignment with behavior. This convergence between empirical measurements and model predictions suggests ventral stream plasticity follows task optimization principles well-approximated by gradient descent, enabling accurate predictions about visual plasticity and generalization to test images.

neuroscience↗

bioRxiv2024

Do Topographic Deep ANN Models of the Primate Ventral Stream Predict the Perceptual Effects of Direct IT Cortical Interventions?

Ever-advancing artificial neural network (ANN) models of the ventral visual stream capture core object recognition behavior and the neural mechanisms underlying it with increasing precision. These models take images as input, propagate through simulated neural representations that resemble biological neural representations at all stages of the primate ventral stream, and produce simulated behavioral choices that resemble primate behavioral choices. We here extend this modeling approach to make and test predictions of neural intervention experiments. Specifically, we enable a new prediction regime for topographic deep ANN (TDANN) models of primate visual processing through the development of perturbation modules that translate micro-stimulation, optogenetic suppression, and muscimol suppression into changes in model neural activity. This unlocks the ability to predict the behavioral effects from particular neural perturbations. We compare these predictions with the key results from the primate IT perturbation experimental literature via a suite of nine corresponding benchmarks. Without any fitting to the benchmarks, we find that TDANN models generated via co-training with both a spatial correlation loss and a standard categorization task qualitatively predict all nine behavioral results. In contrast, TDANN models generated via random topography or via topographic unit arrangement after classification training predict less than half of those results. However, the models quantitative predictions are consistently misaligned with experimental data, over-predicting the magnitude of some behavioral effects and under-predicting others. None of the TDANN models were built with separate model hemispheres and thus, unsurprisingly, all fail to predict hemispheric-dependent effects. Taken together, these findings indicate that current topographic deep ANN models paired with perturbation modules are reasonable guides to predict the qualitative results of direct causal experiments in IT, but that improved TDANN models will be needed for precise quantitative predictions.

neuroscience↗

bioRxiv2023

A Unifying Principle for the Functional Organization of Visual Cortex

A key feature of many cortical systems is functional organization: the arrangement of neurons with specific functional properties in characteristic spatial patterns across the cortical surface. However, the principles underlying the emergence and utility of functional organization are poorly understood. Here we develop the Topographic Deep Artificial Neural Network (TDANN), the first unified model to accurately predict the functional organization of multiple cortical areas in the primate visual system. We analyze the key factors responsible for the TDANNs success and find that it strikes a balance between two specific objectives: achieving a task-general sensory representation that is self-supervised, and maximizing the smoothness of responses across the cortical sheet according to a metric that scales relative to cortical surface area. In turn, the representations learned by the TDANN are lower dimensional and more brain-like than those in models that lack a spatial smoothness constraint. Finally, we provide evidence that the TDANNs functional organization balances performance with inter-area connection length, and use the resulting models for a proof-of-principle optimization of cortical prosthetic design. Our results thus offer a unified principle for understanding functional organization and a novel view of the functional role of the visual system in particular.

neuroscience↗

bioRxiv2023

An empirical assay of view-invariant object learning in humans and comparison with baseline image-computable models

A core problem in visual object learning is using a finite number of images of a new object to accurately identify that object in future, novel images. One longstanding, conceptual hypothesis asserts that this core problem is solved by adult brains through two connected mechanisms: 1) the re-representation of incoming retinal images as points in a fixed, multidimensional neural space, and 2) the optimization of linear decision boundaries in that space, via simple plasticity rules applied to a single downstream layer. Though this scheme is biologically plausible, the extent to which it explains learning behavior in humans has been unclear - in part because of a historical lack of image-computable models of the putative neural space, and in part because of a lack of measurements of human learning behaviors in difficult, naturalistic settings. Here, we addressed these gaps by 1) drawing from contemporary, image-computable models of the primate ventral visual stream to create a large set of testable learning models (n=2,408 models), and 2) using online psychophysics to measure human learning trajectories over a varied set of tasks involving novel 3D objects (n=371,000 trials), which we then used to develop (and publicly release) empirical benchmarks for comparing learning models to humans. We evaluated each learning model on these benchmarks, and found that learning models that using specific, high-level contemporary representations are surprisingly aligned with human behavior. While no tested model explained the entirety of replicable human behavior, these results establish that rudimentary plasticity rules, when combined with appropriate visual representations, have high explanatory power in predicting human behavior with respect to this core object learning problem. Author SummaryA basic conceptual hypothesis for how an adult brain learns to visually identify a new object is: 1) it re-represents images as points in a fixed, multidimensional space, then 2) it learns linear decision boundaries that separate images of a new object from others, using a single layer of plasticity. This hypothesis is considered biologically plausible, but gauging its power to explain human learning behavior has not been straightforward. In part, this is because it is difficult to model how brains re-represent images during object learning. However, ongoing efforts in neuroscience have led to the identification of specific, image-computable models that are at least partially accurate descriptions of the neural representations involved in primate vision. Here, we asked whether any of those representations, when combined them with simple plasticity rules, could make accurate predictions over a large body of human object learning behavioral measurements. We found that specific models could indeed explain a majority of our behavioral measurements, suggesting the rudimentary, biologically-plausible mechanisms considered here may be sufficient to explain a core aspect of human object learning.

animal behavior and cognition↗

bioRxiv2021

Multi-scale hierarchical neural network models that bridge from single neurons in the primate primary visual cortex to object recognition behavior

Primate visual object recognition relies on the representations in cortical areas at the top of the ventral stream that are computed by a complex, hierarchical network of neural populations. While recent work has created reasonably accurate image-computable hierarchical neural network models of those neural stages, those models do not yet bridge between the properties of individual neurons and the overall emergent behavior of the ventral stream. One reason we cannot yet do this is that individual artificial neurons in multi-stage models have not been shown to be functionally similar to individual biological neurons. Here, we took an important first step by building and evaluating hundreds of hierarchical neural network models in how well their artificial single neurons approximate macaque primary visual cortical (V1) neurons. We found that single neurons in certain models are surprisingly similar to their biological counterparts and that the distributions of single neuron properties, such as those related to orientation and spatial frequency tuning, approximately match those in macaque V1. Critically, we observed that hierarchical models with V1 stages that better match macaque V1 at the single neuron level are also more aligned with human object recognition behavior. Finally, we show that an optimized classical neuroscientific model of V1 is more functionally similar to primate V1 than all of the tested multi-stage models, suggesting room for further model improvements with tangible payoffs in closer alignment to human behavior. These results provide the first multi-stage, multi-scale models that allow our field to ask precisely how the specific properties of individual V1 neurons relate to recognition behavior. HighlightsO_LIImage-computable hierarchical neural network models can be naturally extended to create hierarchical "brain models" that allow direct comparison with biological neural networks at multiple scales - from single neurons, to population of neurons, to behavior. C_LIO_LISingle neurons in some of these hierarchical brain models are functionally similar to single neurons in macaque primate visual cortex (V1) C_LIO_LISome hierarchical brain models have processing stages in which the entire distribution of artificial neuron properties closely matches the biological distributions of those same properties in macaque V1 C_LIO_LIHierarchical brain models whose V1 processing stages better match the macaque V1 stage also tend to be more aligned with human object recognition behavior at their output stage C_LI

neuroscience↗

bioRxiv2021

Goal-Driven Recurrent Neural Network Models of the Ventral Visual Stream

The computational role of the abundant feedback connections in the ventral visual stream (VVS) is unclear, enabling humans and non-human primates to effortlessly recognize objects across a multitude of viewing conditions. Prior studies have augmented feedforward convolutional neural networks (CNNs) with recurrent connections to study their role in visual processing; however, often these recurrent networks are optimized directly on neural data or the comparative metrics used are undefined for standard feedforward networks that lack these connections. In this work, we develop task-optimized convolutional recurrent (ConvRNN) network models that more correctly mimic the timing and gross neuroanatomy of the ventral pathway. Properly chosen intermediate-depth ConvRNN circuit architectures, which incorporate mechanisms of feedforward bypassing and recurrent gating, can achieve high performance on a core recognition task, comparable to that of much deeper feedforward networks. We then develop methods that allow us to compare both CNNs and ConvRNNs to fine-grained measurements of primate categorization behavior and neural response trajectories across thousands of stimuli. We find that high performing ConvRNNs provide a better match to this data than feedforward networks of any depth, predicting the precise timings at which each stimulus is behaviorally decoded from neural activation patterns. Moreover, these ConvRNN circuits consistently produce quantitatively accurate predictions of neural dynamics from V4 and IT across the entire stimulus presentation. In fact, we find that the highest performing ConvRNNs, which best match neural and behavioral data, also achieve a strong Pareto-tradeoff between task performance and overall network size. Taken together, our results suggest the functional purpose of recurrence in the ventral pathway is to fit a high performing network in cortex, attaining computational power through temporal rather than spatial complexity.

neuroscience↗

bioRxiv2020

Chronically implantable LED arrays for behavioral optogenetics in primates.

Challenges in behavioral optogenetics in large brains demand development of a chronically implantable platform for light delivery. We have developed Opto-Array, a chronically implantable array of LEDs for high-throughput optogenetic perturbation in non-human primates. We tested the Opto-Array in the primary visual cortex of a macaque monkey, and demonstrated that optogenetic cortical silencing by the Opto-Array results in reliable retinotopic visual deficits on a luminance discrimination task.

neuroscience↗

bioRxiv2020

Simulating a Primary Visual Cortex at the Front of CNNs Improves Robustness to Image Perturbations

Current state-of-the-art object recognition models are largely based on convolutional neural network (CNN) architectures, which are loosely inspired by the primate visual system. However, these CNNs can be fooled by imperceptibly small, explicitly crafted perturbations, and struggle to recognize objects in corrupted images that are easily recognized by humans. Here, by making comparisons with primate neural data, we first observed that CNN models with a neural hidden layer that better matches primate primary visual cortex (V1) are also more robust to adversarial attacks. Inspired by this observation, we developed VOneNets, a new class of hybrid CNN vision models. Each VOneNet contains a fixed weight neural network front-end that simulates primate V1, called the VOneBlock, followed by a neural network back-end adapted from current CNN vision models. The VOneBlock is based on a classical neuroscientific model of V1: the linear-nonlinear-Poisson model, consisting of a biologically-constrained Gabor filter bank, simple and complex cell nonlinearities, and a V1 neuronal stochasticity generator. After training, VOneNets retain high ImageNet performance, but each is substantially more robust, outperforming the base CNNs and state-of-the-art methods by 18% and 3%, respectively, on a conglomerate benchmark of perturbations comprised of white box adversarial attacks and common image corruptions. Finally, we show that all components of the VOneBlock work in synergy to improve robustness. While current CNN architectures are arguably brain-inspired, the results presented here demonstrate that more precisely mimicking just one stage of the primate visual system leads to new gains in ImageNet-level computer vision applications.

neuroscience↗

bioRxiv2020

Fast recurrent processing via ventral prefrontal cortex is needed by the primate ventral stream for robust core visual object recognition

Distributed neural population spiking patterns in macaque inferior temporal (IT) cortex that support core visual object recognition require additional time to develop for specific ("late-solved") images suggesting the necessity of recurrent processing in these computations. Which brain circuit motifs are most responsible for computing and transmitting these putative recurrent signals to IT? To test whether the ventral prefrontal cortex (vPFC) is a critical recurrent circuit node in this system, here we pharmacologically inactivated parts of the vPFC and simultaneously measured IT population activity, while monkeys performed object discrimination tasks. Our results show that vPFC inactivation deteriorated the quality of the late-phase (>150 ms from image onset) IT population code, along with commensurate, specific behavioral deficits for "late-solved" images. Finally, silencing vPFC caused the monkeys IT activity patterns and behavior to become more like those produced by feedforward artificial neural network models of the ventral stream. Together with prior work, these results argue that fast recurrent processing through the vPFC is critical to the production of behaviorally-sufficient object representations in IT.

neuroscience↗

bioRxiv2020

Unsupervised changes in core object recognition behavioral performance are accurately predicted by unsupervised neural plasticity in inferior temporal cortex

Temporal continuity of object identity is a feature of natural visual input, and is potentially exploited -- in an unsupervised manner -- by the ventral visual stream to build the neural representation in inferior temporal (IT) cortex and IT-dependent core object recognition behavior. Here we investigated whether plasticity of individual IT neurons underlies human behavioral changes induced with unsupervised visual experience by building a single-neuron plasticity model combined with a previously established IT population-to-recognition-behavior linking model to predict human learning effects. We found that our model quite accurately predicted the mean direction, magnitude and time course of human performance changes. We also found a previously unreported dependency of the observed human performance change on the initial task difficulty. This result adds support to the hypothesis that tolerant core object recognition in human and non-human primates is instructed -- at least in part -- by naturally occurring unsupervised temporal contiguity experience.

neuroscience↗

bioRxiv2019

A potential cortical precursor of visual word form recognition in untrained monkeys

Skilled human readers can readily recognize written letters and letter strings. This domain of visual recognition, known as orthographic processing, is foundational to human reading, but it is unclear how it is supported by neural populations in the human brain. Behavioral research has shown that non-human primates (baboons) can learn to distinguish written English words from pseudo-words (lexical decision), successfully generalize that behavior to novel strings, and exhibit behavioral error patterns that are consistent with humans. Thus, non-human primate models, while not capturing the entirety of human reading abilities, may provide a unique opportunity to investigate the neuronal mechanisms underlying orthographic processing. Here, we investigated the neuronal representation of letters and letter strings in the ventral visual stream of naive macaque monkeys, and asked to what extent these representations could support visual word recognition. We recorded the activity of hundreds of neurons at the top two levels of the ventral visual form processing pathway (V4 and IT) while monkeys passively viewed images of letters, English words, and non-word letter strings. Linear decoders were used to probe whether those neural responses could support a battery of orthographic processing tasks such as invariant letter identification and lexical decision. We found that IT-based decoders achieved baboon-level performance on these tasks, with a pattern of errors highly correlated to the previously reported primate behavior. This capacity to support orthographic processing tasks was also present in the high-layer units of state-of-the-art artificial neural network models of the ventral stream, but not in the low-layer representations of those models. Taken together, these results show that the IT cortex of untrained monkeys contains a reservoir of precursor features from which downstream brain regions could, with some supervised instruction, learn to support the visual recognition of written words. This suggests that the acquisition of reading in humans did not require a full rebuild of visual processing, but rather the recycling of a brain network evolved for other visual functions.

neuroscience↗

bioRxiv2019

To find better neural network models of human vision, find better neural network models of primate vision

Specific deep artificial neural networks (ANNs) are the current best models of ventral visual processing and object recognition behavior in monkeys. We here explore whether models of non-human primate vision generalize to visual processing in the human primate brain. Specifically, we asked if model match to monkey IT is a predictor of model match to human IT, even when scoring those matches on different images. We found that the model match to monkey IT is a positive predictor of the model match to human IT (R = 0.36), and that this approach outperforms the current standard predictor of model accuracy on ImageNet. This suggests a more powerful approach for pre-selecting models as hypotheses of human brain processing.

neuroscience↗

bioRxiv2018

Brain-Score: Which Artificial Neural Network for Object Recognition is most Brain-Like?

The internal representations of early deep artificial neural networks (ANNs) were found to be remarkably similar to the internal neural representations measured experimentally in the primate brain. Here we ask, as deep ANNs have continued to evolve, are they becoming more or less brain-like? ANNs that are most functionally similar to the brain will contain mechanisms that are most like those used by the brain. We therefore developed Brain-Score - a composite of multiple neural and behavioral benchmarks that score any ANN on how similar it is to the brains mechanisms for core object recognition - and we deployed it to evaluate a wide range of state-of-the-art deep ANNs. Using this scoring system, we here report that: (1) DenseNet-169, CORnet-S and ResNet-101 are the most brain-like ANNs. (2) There remains considerable variability in neural and behavioral responses that is not predicted by any ANN, suggesting that no ANN model has yet captured all the relevant mechanisms. (3) Extending prior work, we found that gains in ANN ImageNet performance led to gains on Brain-Score. However, correlation weakened at [≥] 70% top-1 ImageNet performance, suggesting that additional guidance from neuroscience is needed to make further advances in capturing brain mechanisms. (4) We uncovered smaller (i.e. less complex) ANNs that are more brain-like than many of the best-performing ImageNet models, which suggests the opportunity to simplify ANNs to better understand the ventral stream. The scoring system used here is far from complete. However, we propose that evaluating and tracking model-benchmark correspondences through a Brain-Score that is regularly updated with new brain data is an exciting opportunity: experimental benchmarks can be used to guide machine network evolution, and machine networks are mechanistic hypotheses of the brains network and thus drive next experiments. To facilitate both of these, we release Brain-Score.org: a platform that hosts the neural and behavioral benchmarks, where ANNs for visual processing can be submitted to receive a Brain-Score and their rank relative to other models, and where new experimental data can be naturally incorporated.

neuroscience↗

bioRxiv2018

CORnet: Modeling the Neural Mechanisms of Core Object Recognition

Deep artificial neural networks with spatially repeated processing (a.k.a., deep convolutional ANNs) have been established as the best class of candidate models of visual processing in primate ventral visual processing stream. Over the past five years, these ANNs have evolved from a simple feedforward eight-layer architecture in AlexNet to extremely deep and branching NAS-Net architectures, demonstrating increasingly better object categorization performance and increasingly better explanatory power of both neural and behavioral responses. However, from the neuroscientists point of view, the relationship between such very deep architectures and the ventral visual pathway is incomplete in at least two ways. On the one hand, current state-of-the-art ANNs appear to be too complex (e.g., now over 100 levels) compared with the relatively shallow cortical hierarchy (4-8 levels), which makes it difficult to map their elements to those in the ventral visual stream and to understand what they are doing. On the other hand, current state-of-the-art ANNs appear to be not complex enough in that they lack recurrent connections and the resulting neural response dynamics that are commonplace in the ventral visual stream. Here we describe our ongoing efforts to resolve both of these issues by developing a \"CORnet\" family of deep neural network architectures. Rather than just seeking high object recognition performance (as the state-of-the-art ANNs above), we instead try to reduce the model family to its most important elements and then gradually build new ANNs with recurrent and skip connections while monitoring both performance and the match between each new CORnet model and a large body of primate brain and behavioral data. We report here that our current best ANN model derived from this approach (CORnet-S) is among the top models on Brain-Score, a composite benchmark for comparing models to the brain, but is simpler than other deep ANNs in terms of the number of convolutions performed along the longest path of information processing in the model. All CORnet models are available at github.com/dicarlolab/CORnet, and we plan to up-date this manuscript and the available models in this family as they are produced.

neuroscience↗

bioRxiv2018

Reversible inactivation of different millimeter-scale regions of primate IT results in different patterns of core object recognition deficits

Extensive research suggests that the inferior temporal (IT) population supports visual object recognition behavior. However, causal evidence for this hypothesis has been equivocal, particularly beyond the specific case of face-selective sub-regions of IT. Here, we directly tested this hypothesis by pharmacologically inactivating individual, millimeter-scale sub-regions of IT while monkeys performed several object discrimination tasks, interleaved trial-by-trial. First, we observed that IT inactivation resulted in reliable contralateral-biased task-selective behavioral deficits. Moreover, inactivating different IT sub-regions resulted in different patterns of task deficits, each predicted by that sub-regions neuronal object discriminability. Finally, the similarity between different inactivation effects was tightly related to the anatomical distance between corresponding inactivation sites. Taken together, these results provide direct evidence that IT cortex causally supports general core object recognition, and that the underlying IT codes are topographically organized.

neuroscience↗

bioRxiv2018

Evidence that recurrent circuits are critical to the ventral stream’s execution of core object recognition behavior

Non-recurrent deep convolutional neural networks (DCNNs) are currently the best models of core object recognition; a behavior supported by the densely recurrent primate ventral stream, culminating in the inferior temporal (IT) cortex. Are these recurrent circuits critical to ventral streams execution of this behavior? We reasoned that, if recurrence is critical, then primates should outperform feedforward-only DCNNs for some images, and that these images should require additional processing time beyond the feedforward IT response. Here we first used behavioral methods to discover hundreds of these \"challenge\" images. Second, using large-scale IT electrophysiology in animals performing core recognition tasks, we observed that behaviorally-sufficient, linearly-decodable object identity solutions emerged ~30ms (on average) later in IT for challenge images compared to DCNN and primate performance-matched \"control\" images. We observed these same late solutions even during passive viewing. Third, consistent with a failure of feedforward computations, the behaviorally-critical late-phase IT population response patterns evoked by the challenge images were poorly predicted by DCNN activations. Interestingly, deeper CNNs better predicted these late IT responses, suggesting a functional equivalence between recurrence and additional nonlinear transformations. Our results argue that automatically-evoked recurrent circuits are critical even for rapid object identification. By precisely comparing current DCNNs, primate behavior and IT population dynamics, we provide guidance for future recurrent model development.

neuroscience↗

bioRxiv2018

Large-scale, high-resolution comparison of the core visual object recognition behavior of humans, monkeys, and state-of-the-art deep artificial neural networks

Primates--including humans--can typically recognize objects in visual images at a glance even in the face of naturally occurring identity-preserving image transformations (e.g. changes in viewpoint). A primary neuroscience goal is to uncover neuron-level mechanistic models that quantitatively explain this behavior by predicting primate performance for each and every image. Here, we applied this stringent behavioral prediction test to the leading mechanistic models of primate vision (specifically, deep, convolutional, artificial neural networks; ANNs) by directly comparing their behavioral signatures against those of humans and rhesus macaque monkeys. Using high-throughput data collection systems for human and monkey psychophysics, we collected over one million behavioral trials for 2400 images over 276 binary object discrimination tasks. Consistent with previous work, we observed that state-of-the-art deep, feed-forward convolutional ANNs trained for visual categorization (termed DCNNIC models) accurately predicted primate patterns of object-level confusion. However, when we examined behavioral performance for individual images within each object discrimination task, we found that all tested DCNNIC models were significantly non-predictive of primate performance, and that this prediction failure was not accounted for by simple image attributes, nor rescued by simple model modifications. These results show that current DCNNIC models cannot account for the image-level behavioral patterns of primates, and that new ANN models are needed to more precisely capture the neural mechanisms underlying primate object vision. To this end, large-scale, high-resolution primate behavioral benchmarks--such as those obtained here--could serve as direct guides for discovering such models.\n\nSIGNIFICANCE STATEMENTRecently, specific feed-forward deep convolutional artificial neural networks (ANNs) models have dramatically advanced our quantitative understanding of the neural mechanisms underlying primate core object recognition. In this work, we tested the limits of those ANNs by systematically comparing the behavioral responses of these models with the behavioral responses of humans and monkeys, at the resolution of individual images. Using these high-resolution metrics, we found that all tested ANN models significantly diverged from primate behavior. Going forward, these high-resolution, large-scale primate behavioral benchmarks could serve as direct guides for discovering better ANN models of the primate visual system.

neuroscience↗

bioRxiv2017

Deep brain fluorescence imaging with minimally invasive ultra-thin optical fibers

A major open challenge in neuroscience is the ability to measure and perturb neural activity in vivo from well-defined neural sub-populations at cellular resolution anywhere in the brain. However, limitations posed by scattering and absorption prohibit non-invasive (surface) multiphoton approaches1,2 for deep (>2mm) structures, while Gradient Refreactive Index (GRIN) endoscopes2-4 are thick and cause significant damage upon insertion. Here, we demonstrate a novel microendoscope to image neural activity at arbitrary depths via an ultrathin multimode optical fiber (MMF) probe that is 5-10X thinner than commercially available microendoscopes. We demonstrate micron-scale resolution, multispectral and volumetric imaging. In contrast to previous approaches1,5-8 we show that this method has an improved acquisition speed that is sufficient to capture rapid neuronal dynamics in-vivo in rodents expressing a genetically encoded calcium indicator. Our results emphasize the potential of this technology in neuroscience applications and open up possibilities for cellular resolution imaging in previously unreachable brain regions.

neuroscience↗