%0 Journal Article %J eLife %D 2018 %T Neural dynamics at successive stages of the ventral visual stream are consistent with hierarchical error signals. %A Issa, Elias B %A Cadieu, Charles F %A DiCarlo, James J %K Animals %K Brain Mapping %K Face %K Humans %K Macaca mulatta %K Models %K Neurological %K Neurons %K Pattern Recognition %K Photic Stimulation %K Reaction Time %K Visual %K Visual Cortex %K Visual Perception %X

Ventral visual stream neural responses are dynamic, even for static image presentations. However, dynamical neural models of visual cortex are lacking as most progress has been made modeling static, time-averaged responses. Here, we studied population neural dynamics during face detection across three cortical processing stages. Remarkably,~30 milliseconds after the initially evoked response, we found that neurons in intermediate level areas decreased their responses to typical configurations of their preferred face parts relative to their response for atypical configurations even while neurons in higher areas achieved and maintained a preference for typical configurations. These hierarchical neural dynamics were inconsistent with standard feedforward circuits. Rather, recurrent models computing prediction errors between stages captured the observed temporal signatures. This model of neural dynamics, which simply augments the standard feedforward model of online vision, suggests that neural responses to static images may encode top-down prediction errors in addition to bottom-up feature estimates.

%B eLife %V 7 %8 11/2018 %G eng %U https://elifesciences.org/articles/42870https://cdn.elifesciences.org/articles/42870/elife-42870-v2.pdf %R 10.7554/eLife.42870 %0 Journal Article %J Journal of Neuroscience %D 2005 %T Multiple Object Response Normalization in Monkey Inferotemporal Cortex %A Zoccolan, D. %A Cox, David D. %A DiCarlo, James J. %K Animals %K Brain Mapping %K Macaca mulatta %K Male %K Photic Stimulation %K Posture %K Psychology %K Recognition %K Temporal Lobe %K Visual Pathways %K Visual Perception %X

The highest stages of the visual ventral pathway are commonly assumed to provide robust representation of object identity by disregarding confounding factors such as object position, size, illumination, and the presence of other objects (clutter). However, whereas neuronal responses in monkey inferotemporal cortex (IT) can show robust tolerance to position and size changes, previous work shows that responses to preferred objects are usually reduced by the presence of nonpreferred objects. More broadly, we do not yet understand multiple object representation in IT. In this study, we systematically examined IT responses to pairs and triplets of objects in three passively viewing monkeys across a broad range of object effectiveness. We found that, at least under these limited clutter conditions, a large fraction of the response of each IT neuron to multiple objects is reliably predicted as the average of its responses to the constituent objects in isolation. That is, multiple object responses depend primarily on the relative effectiveness of the constituent objects, regardless of object identity. This average effect becomes virtually perfect when populations of IT neurons are pooled. Furthermore, the average effect cannot simply be explained by attentional shifts but behaves as a primarily feedforward response property. Together, our observations are most consistent with mechanistic models in which IT neuronal outputs are normalized by summed synaptic drive into IT or spiking activity within IT and suggest that normalization mechanisms previously revealed at earlier visual areas are operating throughout the ventral visual stream.

%B Journal of Neuroscience %V 25 %P 8150 - 8164 %8 07/2005 %G eng %U http://www.jneurosci.org/cgi/doi/10.1523/JNEUROSCI.2058-05.2005 %N 36 %! Journal of Neuroscience %R 10.1523/JNEUROSCI.2058-05.2005 %0 Journal Article %J Journal of Neurophysiology %D 2004 %T Using Neuronal Latency to Determine Sensory–Motor Processing Pathways in Reaction Time Tasks %A DiCarlo, James J. %A Maunsell, John H. R. %K Action Potentials %K Afferent %K Animal %K Animals %K Behavior %K Macaca mulatta %K Male %K Models %K Motor Neurons %K Neural Pathways %K Neurological %K Neurons %K Photic Stimulation %K Psychomotor Performance %K Reaction Time %K Task Performance and Analysis %K Temporal Lobe %K Time Factors %K Visual Fields %X

We describe a new technique that uses the timing of neuronal and behavioral responses to explore the contributions of individual neurons to specific behaviors. The approach uses both the mean neuronal latency and the trial-by-trial covariance between neuronal latency and behavioral response. Reliable measurements of these values were obtained from single-unit recordings made from anterior inferotemporal (AIT) cortex and the frontal eye fields (FEF) in monkeys while they performed a choice reaction time task. These neurophysiological data show that the responses of AIT neurons and some FEF neurons have little covariance with behavioral response, consistent with a largely "sensory" response. The responses of another group of FEF neurons with longer mean latency covary tightly with behavioral response, consistent with a largely "motor" response. A very small fraction of FEF neurons had responses consistent with an intermediate position in the sensory-motor pathway. These results suggest that this technique is a valuable tool for exploring the functional organization of neuronal circuits that underlie specific behaviors.

 

%B Journal of Neurophysiology %V 93 %P 2974 - 2986 %8 11/2004 %G eng %U https://www.physiology.org/doi/10.1152/jn.00508.2004 %N 5 %! Journal of Neurophysiology %R 10.1152/jn.00508.2004 %0 Journal Article %J Journal of Neurophysiology %D 2003 %T Anterior Inferotemporal Neurons of Monkeys Engaged in Object Recognition Can be Highly Sensitive to Object Retinal Position %A DiCarlo, James J. %A Maunsell, John H. R. %K Action Potentials %K Animals %K Depth Perception %K Electrophysiology %K Eye Movements %K Form Perception %K Macaca mulatta %K Male %K Neurons %K Pattern Recognition %K Photic Stimulation %K Psychomotor Performance %K Retina %K Temporal Lobe %K Time Factors %K Visual %K Visual Fields %K Visual Perception %X

Visual object recognition is computationally difficult because changes in an object's position, distance, pose, or setting may cause it to produce a different retinal image on each encounter. To robustly recognize objects, the primate brain must have mechanisms to compensate for these variations. Although these mechanisms are poorly understood, it is thought that they elaborate neuronal representations in the inferotemporal cortex that are sensitive to object form but substantially invariant to other image variations. This study examines this hypothesis for image variation resulting from changes in object position. We studied the effect of small differences (+/-1.5 degrees ) in the retinal position of small (0.6 degrees wide) visual forms on both the behavior of monkeys trained to identify those forms and the responses of 146 anterior IT (AIT) neurons collected during that behavior. Behavioral accuracy and speed were largely unaffected by these small changes in position. Consistent with previous studies, many AIT responses were highly selective for the forms. However, AIT responses showed far greater sensitivity to retinal position than predicted from their reported receptive field (RF) sizes. The median AIT neuron showed a approximately 60% response decrease between positions within +/-1.5 degrees of the center of gaze, and 52% of neurons were unresponsive to one or more of these positions. Consistent with previous studies, each neuron's rank order of target preferences was largely unaffected across position changes. Although we have not yet determined the conditions necessary to observe this marked position sensitivity in AIT responses, we rule out effects of spatial-frequency content, eye movements, and failures to include the RF center. To reconcile this observation with previous studies, we hypothesize that either AIT position sensitivity strongly depends on object size or that position sensitivity is sharpened by extensive visual experience at fixed retinal positions or by the presence of flanking distractors.

 

%B Journal of Neurophysiology %V 89 %P 3264 - 3278 %8 01/2003 %G eng %U https://www.physiology.org/doi/10.1152/jn.00358.2002 %N 6 %! Journal of Neurophysiology %R 10.1152/jn.00358.2002 %0 Journal Article %J Nature Neuroscience %D 2000 %T Form representation in monkey inferotemporal cortex is virtually unaltered by free viewing %A DiCarlo, James J. %A Maunsell, John H. R. %K Animals %K Conditioning %K Fixation %K Form Perception %K Macaca mulatta %K Male %K Neurons %K Ocular %K Pattern Recognition %K Photic Stimulation %K Psychology %K Saccades %K Temporal Lobe %K Visual %K Visual Cortex %X

How are objects represented in the brain during natural behavior? Visual object recognition in primates is thought to depend on the inferotemporal cortex {(IT).} In most neurophysiological studies of {IT,} monkeys hold their direction of gaze fixed while isolated visual stimuli are presented (controlled viewing). However, during natural behavior, primates visually explore cluttered environments by changing gaze direction several times each second (free viewing). We examined the effect of free viewing on {IT} neuronal responses in monkeys engaged in a form-recognition task. By making small, real-time stimulus adjustments, we produced nearly identically retinal stimulation during controlled and free viewing. Nearly 90% of neuronal responses were unaffected by free viewing, and average stimulus selectivity was unchanged. Thus, neuronal representations that likely underlie form recognition are virtually unaltered by free viewing.

%B Nature Neuroscience %V 3 %P 814 - 821 %8 01/2000 %G eng %U http://www.nature.com/articles/nn0800_814 %N 8 %! Nat Neurosci %R 10.1038/77722