Davide Zoccolan

Multiple Object Response Normalization in Monkey Inferotemporal Cortex

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.

Trade-Off between Object Selectivity and Tolerance in Monkey Inferotemporal Cortex

Object recognition requires both selectivity among different objects and tolerance to vastly different retinal images of the same object, resulting from natural variation in (e.g.) position, size, illumination, and clutter. Thus, discovering neuronal responses that have object selectivity and tolerance to identity-preserving transformations is fundamental to understanding object recognition. Although selectivity and tolerance are found at the highest level of the primate ventral visual stream [the inferotemporal cortex (IT)], both properties are highly varied and poorly understood. If an IT neuron has very sharp selectivity for a unique combination of object features (“diagnostic features”), this might automatically endow it with high tolerance. However, this relationship cannot be taken as given; although some IT neurons are highly object selective and some are highly tolerant, the empirical connection of these key properties is unknown. In this study, we systematically measured both object selectivity and tolerance to different identity-preserving image transformations in the spiking responses of a population of monkey IT neurons. We found that IT neurons with high object selectivity typically have low tolerance (and vice versa), regardless of how object selectivity was quantified and the type of tolerance examined. The discovery of this trade-off illuminates object selectivity and tolerance in IT and unifies a range of previous, seemingly disparate results. This finding also argues against the idea that diagnostic conjunctions of features guarantee tolerance. Instead, it is naturally explained by object recognition models in which object selectivity is built through AND-like tuning mechanisms.

Shape Similarity, Better than Semantic Membership, Accounts for the Structure of Visual Object Representations in a Population of Monkey Inferotemporal Neurons

The anterior inferotemporal cortex (IT) is the highest stage along the hierarchy of visual areas that, in primates, processes visual objects. Although several lines of evidence suggest that IT primarily represents visual shape information, some recent studies have argued that neuronal ensembles in IT code the semantic membership of visual objects (i.e., represent conceptual classes such as animate and inanimate objects). In this study, we investigated to what extent semantic, rather than purely visual information, is represented in IT by performing a multivariate analysis of IT responses to a set of visual objects. By relying on a variety of machine-learning approaches (including a cutting-edge clustering algorithm that has been recently developed in the domain of statistical physics), we found that, in most instances, IT representation of visual objects is accounted for by their similarity at the level of shape or, more surprisingly, low-level visual properties. Only in a few cases we observed IT representations of semantic classes that were not explainable by the visual similarity of their members. Overall, these findings reassert the primary function of IT as a conveyor of explicit visual shape information, and reveal that low-level visual properties are represented in IT to a greater extent than previously appreciated. In addition, our work demonstrates how combining a variety of state-of-the-art multivariate approaches, and carefully estimating the contribution of shape similarity to the representation of object categories, can substantially advance our understanding of neuronal coding of visual objects in cortex.

Multifeatural Shape Processing in Rats Engaged in Invariant Visual Object Recognition

The ability to recognize objects despite substantial variation in their appearance (e.g., because of position or size changes) represents such a formidable computational feat that it is widely assumed to be unique to primates. Such an assumption has restricted the investigation of its neuronal underpinnings to primate studies, which allow only a limited range of experimental approaches. In recent years, the increasingly powerful array of optical and molecular tools that has become available in rodents has spurred a renewed interest for rodent models of visual functions. However, evidence of primate-like visual object processing in rodents is still very limited and controversial. Here we show that rats are capable of an advanced recognition strategy, which relies on extracting the most informative object features across the variety of viewing conditions the animals may face. Rat visual strategy was uncovered by applying an image masking method that revealed the features used by the animals to discriminate two objects across a range of sizes, positions, in-depth, and in-plane rotations. Noticeably, rat recognition relied on a combination of multiple features that were mostly preserved across the transformations the objects underwent, and largely overlapped with the features that a simulated ideal observer deemed optimal to accomplish the discrimination task. These results indicate that rats are able to process and efficiently use shape information, in a way that is largely tolerant to variation in object appearance. This suggests that their visual system may serve as a powerful model to study the neuronal substrates of object recognition.

Transformation-Tolerant Object Recognition in Rats Revealed by Visual Priming

Successful use of rodents as models for studying object vision crucially depends on the ability of their visual system to construct representations of visual objects that tolerate (i.e., remain relatively unchanged with respect to) the tremendous changes in object appearance produced, for instance, by size and viewpoint variation. Whether this is the case is still controversial, despite some recent demonstration of transformation-tolerant object recognition in rats. In fact, it remains unknown to what extent such a tolerant recognition has a spontaneous, perceptual basis, or, alternatively, mainly reflects learning of arbitrary associative relations among trained object appearances. In this study, we addressed this question by training rats to categorize a continuum of morph objects resulting from blending two object prototypes. The resulting psychometric curve (reporting the proportion of responses to one prototype along the morph line) served as a reference when, in a second phase of the experiment, either prototype was briefly presented as a prime, immediately before a test morph object. The resulting shift of the psychometric curve showed that recognition became biased toward the identity of the prime. Critically, this bias was observed also when the primes were transformed along a variety of dimensions (i.e., size, position, viewpoint, and their combination) that the animals had never experienced before. These results indicate that rats spontaneously perceive different views/appearances of an object as similar (i.e., as instances of the same object) and argue for the existence of neuronal substrates underlying formation of transformation-tolerant object representations in rats.

A self-calibrating, camera-based eye tracker for the recording of rodent eye movements

Much of neurophysiology and vision science relies on careful measurement of a human or animal subjects gaze direction. Video-based eye trackers have emerged as an especially popular option for gaze tracking, because they are easy to use and are completely non-invasive. However, video eye trackers typically require a calibration procedure in which the subject must look at a series of points at known gaze angles. While it is possible to rely on innate orienting behaviors for calibration in some non-human species, other species, such as rodents, do not reliably saccade to visual targets, making this form of calibration impossible. To overcome this problem, we developed a fully automated infrared video eye-tracking system that is able to quickly and accurately calibrate itself without requiring co-operation from the subject. This technique relies on the optical geometry of the cornea and uses computer-controlled motorized stages to rapidly estimate the geometry of the eye relative to the camera. The accuracy and precision of our system was carefully measured using an artificial eye, and its capability to monitor the gaze of rodents was verified by tracking spontaneous saccades and evoked oculomotor reflexes in head-fixed rats (in both cases, we obtained measurements that are consistent with those found in the literature). Overall, given its fully automated nature and its intrinsic robustness against operator errors, we believe that our eye-tracking system enhances the utility of existing approaches to gaze-tracking in rodents and represents a valid tool for rodent vision studies.

Interneurone bursts are spontaneously associated with muscle contractions only during early phases of mouse spinal network development: a study in organotypic cultures

For a short time during development immature circuits in the spinal cord and other parts of the central nervous system spontaneously generate synchronous patterns of rhythmic activity. In the case of the spinal cord, it is still unclear how strongly synchronized bursts generated by interneurones are associated with motoneurone firing and whether the progressive decline in spontaneous bursting during circuit maturation proceeds in parallel for motoneurone and interneurone networks. We used organotypic cocultures of spinal cord and skeletal muscle in order to investigate the ontogenic evolution of endogenous spinal network activity associated with the generation of coordinate muscle fibre contractions. A combination of multiunit electrophysiological recordings, videomicroscopy and optical flow computation allowed us to measure the correlation between interneurone firing and motoneurone outputs after 1, 2 and 3 weeks of in vitro development. We found that, in spinal organotypic slices, there is a developmental switch of spontaneous activity from stable bursting to random patterns after the first week in culture. Conversely, bursting recorded in the presence of strychnine and bicuculline became increasingly regular with time in vitro. The time course of spontaneous activity maturation in organotypic slices is similar to that previously reported for the spinal cord developing in utero. We also demonstrated that spontaneous bursts of interneurone action potentials strongly correlate with muscular contractions only during the first week in vitro and that this is due to the activation of motoneurones via AMPA‐type glutamate receptors. These results indicate the occurrence in vitro of motor network development regulating bursting inputs from interneurones to motoneurones.

The use of optical flow to characterize muscle contraction.

Muscle contraction is usually measured and characterized with force and displacement transducers. The contraction of muscle fibers, however, evokes in the tissue a two and even three-dimensional displacement field, which is not properly quantified by these transducers because they provide just a single scalar quantity. This problem can be circumvented by using optical measurements and standard tools of computer vision, developed for the analysis of time varying image sequences. By computing the so called optical flow, i.e. the apparent motion of points in a time varying image sequence, it is possible to recover a two-dimensional motion field, describing rather precisely the displacement caused by muscle contraction in a flattened piece of skin. The obtained two-dimensional optical flow can be further analyzed by computing its elementary deformation components, providing a novel and accurate characterization of the contraction induced by different motoneurons. This technique is demonstrated analyzing the displacement caused by muscle contraction in the skin of the leech, Hirudo medicinalis. The proposed technique can be applied to monitor and characterize all contractions in almost flat tissues with enough visual texture.

Invariant visual object recognition and shape processing in rats

Highlights • Rats are capable of invariant visual object recognition.• Rats spontaneously perceive different views of a visual object as similar to each other, that is as instances of the same object.• Rats are capable of a multifeatural, shape-based visual processing strategy.• Rats can learn complex, configural visual discriminations.• Rats spontaneously process composite visual patterns according to perceptual grouping cues.

Statistics of Decision Making in the Leech

Animals continuously decide among different behaviors, but, even in invertebrates, the mechanisms underlying choice and decision are unknown. In this article, leech spontaneous behavior was tracked and quantified for up to 12 h. We obtained a statistical characterization, in space and time domains, of the decision processes underlying selection of behavior in the leech. We found that the spatial distribution of leech position in a uniform environment is isotropic (the same in all directions), but this isotropy is broken in the presence of localized external stimuli. In the time domain, transitions among behaviors can be described by a Markov process, the structure of which (allowed states and transitions) is highly conserved across individuals. Finally, a wide range of recurrent, deterministic motifs was identified in the apparently irregular and unstructured exploratory behavior. These results provide a rigorous description of the inner dynamics that control the spontaneous and continuous flow of behavioral decisions in the leech.