Maxime Cauchoix

The Neural Dynamics of Face Detection in the Wild Revealed by MVPA

Previous magnetoencephalography/electroencephalography (M/EEG) studies have suggested that face processing is extremely rapid, indeed faster than any other object category. Most studies, however, have been performed using centered, cropped stimuli presented on a blank background resulting in artificially low interstimulus variability. In contrast, the aim of the present study was to assess the underlying temporal dynamics of face detection presented in complex natural scenes. We recorded EEG activity while participants performed a rapid go/no-go categorization task in which they had to detect the presence of a human face. Subjects performed at ceiling (94.8% accuracy), and traditional event-related potential analyses revealed only modest modulations of the two main components classically associated with face processing (P100 and N170). A multivariate pattern analysis conducted across all EEG channels revealed that face category could, however, be readout very early, under 100 ms poststimulus onset. Decoding was linked to reaction time as early as 125 ms. Decoding accuracy did not increase monotonically; we report an increase during an initial 95–140 ms period followed by a plateau ∼140–185 ms–perhaps reflecting a transitory stabilization of the face information available–and a strong increase afterward. Further analyses conducted on individual images confirmed these phases, further suggesting that decoding accuracy may be initially driven by low-level stimulus properties. Such latencies appear to be surprisingly short given the complexity of the natural scenes and the large intraclass variability of the face stimuli used, suggesting that the visual system is highly optimized for the processing of natural scenes.

Humans and monkeys share visual representations

Conceptual abilities in animals have been shown at several levels of abstraction, but it is unclear whether the analogy with humans results from convergent evolution or from shared brain mechanisms inherited from a common origin. Macaque monkeys can access “non-similarity–based concepts,” such as when sorting pictures containing a superordinate target category (animal, tree, etc.) among other scenes. However, such performances could result from low-level visual processing based on learned regularities of the photographs, such as for scene categorization by artificial systems. By using pictures of man-made objects or animals embedded in man-made or natural contexts, the present study clearly establishes that macaque monkeys based their categorical decision on the presence of the animal targets regardless of the scene backgrounds. However, as is found with humans, monkeys performed better with categorically congruent object/context associations, especially when small object sizes favored background information. The accuracy improvements and the response-speed gains attributable to superordinate category congruency in monkeys were strikingly similar to those of human subjects tested with the same task and stimuli. These results suggest analogous processing of visual information during the activation of abstract representations in both humans and monkeys; they imply a large overlap between superordinate visual representations in humans and macaques as well as the implicit use of experienced associations between object and context.

How plausible is a subcortical account of rapid visual recognition

Primates recognize objects in natural visual scenes with great rapidity. The ventral visual cortex is usually assumed to play a major role in this ability (“high-road”). However, the “low-road” alternative frequently proposed is that the visual cortex is bypassed by a rapid subcortical route to the amygdala, especially in the case of biologically relevant and emotional stimuli. This paper highlights the lack of evidence from psychophysics and computational models to support this “low-road” alternative. Most importantly, the timing of neural responses invites a serious reconsideration of the low-road role in rapid processing of visual objects.

How Can We Study the Evolution of Animal Minds

During the last 50 years, comparative cognition and neurosciences have improved our understanding of animal minds while evolutionary ecology has revealed how selection acts on traits through evolutionary time. We describe how cognition can be subject to natural selection like any other biological trait and how this evolutionary approach can be used to understand the evolution of animal cognition. We recount how comparative and fitness methods have been used to understand the evolution of cognition and outline how these approaches could extend our understanding of cognition. The fitness approach, in particular, offers unprecedented opportunities to study the evolutionary mechanisms responsible for variation in cognition within species and could allow us to investigate both proximate (i.e., neural and developmental) and ultimate (i.e., ecological and evolutionary) underpinnings of animal cognition together. We highlight recent studies that have successfully shown that cognitive traits can be under selection, in particular by linking individual variation in cognition to fitness. To bridge the gap between cognitive variation and fitness consequences and to better understand why and how selection can occur on cognition, we end this review by proposing a more integrative approach to study contemporary selection on cognitive traits combining socio-ecological data, minimally invasive neuroscience methods and measurement of ecologically relevant behaviors linked to fitness. Our overall goal in this review is to build a bridge between cognitive neuroscientists and evolutionary biologists, illustrate how their research could be complementary, and encourage evolutionary ecologists to include explicit attention to cognitive processes in their studies of behavior.

Fast ventral stream neural activity enables rapid visual categorization

Primates can recognize objects embedded in complex natural scenes in a glimpse. Rapid categorization paradigms have been extensively used to study our core perceptual abilities when the visual system is forced to operate under strong time constraints. However, the neural underpinning of rapid categorization remains to be understood, and the incredible speed of sight has yet to be reconciled with modern ventral stream cortical theories of object recognition. Here we recorded multichannel subdural electrocorticogram (ECoG) signals from intermediate areas (V4/PIT) of the ventral stream of the visual cortex while monkeys were actively engaged in a rapid animal/non-animal categorization task. A traditional event-related potential (ERP) analysis revealed short visual latencies (<50-70ms) followed by a rapidly developing visual selectivity (within ~20-30ms) for most electrodes. A multi-variate pattern analysis (MVPA) technique further confirmed that reliable animal/non-animal category information was possible from this initial ventral stream neural activity (within ~90-100ms). Furthermore, this early category-selective neural activity was (a) unaffected by the presentation of a backward (pattern) mask, (b) generalized to novel (unfamiliar) stimuli and (c) co-varied with behavioral responses (both accuracy and reaction times). Despite the strong prevalence of task-related information on the neural signal, task-irrelevant visual information could still be decoded independently of monkey behavior. Monkey behavioral responses were also found to correlate significantly with human behavioral responses for the same set of stimuli. Together, the present study establishes that rapid ventral stream neural activity induces a visually selective signal subsequently used to drive rapid visual categorization and that this visual strategy may be shared between human and non-human primates.

The repeatability of cognitive performance: a meta-analysis

Behavioural and cognitive processes play important roles in mediating an individuals interactions with its environment. Yet, while there is a vast literature on repeatable individual differences in behaviour, relatively little is known about the repeatability of cognitive performance. To further our understanding of the evolution of cognition, we gathered 44 studies on individual performance of 25 species across six animal classes and used meta-analysis to assess whether cognitive performance is repeatable. We compared repeatability (R) in performance (1) on the same task presented at different times (temporal repeatability), and (2) on different tasks that measured the same putative cognitive ability (contextual repeatability). We also addressed whether R estimates were influenced by seven extrinsic factors (moderators): type of cognitive performance measurement, type of cognitive task, delay between tests, origin of the subjects, experimental context, taxonomic class and publication status. We found support for both temporal and contextual repeatability of cognitive performance, with mean R estimates ranging between 0.15 and 0.28. Repeatability estimates were mostly influenced by the type of cognitive performance measures and publication status. Our findings highlight the widespread occurrence of consistent inter-individual variation in cognition across a range of taxa which, like behaviour, may be associated with fitness outcomes. This article is part of the theme issue ‘Causes and consequences of individual differences in cognitive abilities’.

The neural dynamics of visual processing in monkey extrastriate cortex: a comparison between univariate and multivariate techniques

Understanding the brain mechanisms underlying invariant visual recognition has remained a central tenet of cognitive neuroscience. Much of our current understanding of this process is based on knowledge gained from visual areas studied individually. Previous electrophysiology studies have emphasized the role of the ventral stream of the visual cortex in shape processing and, in particular, of higher level visual areas in encoding abstract category information. Surprisingly, relatively little is known about the precise dynamics of visual processing along the ventral stream of the visual cortex. Here we recorded intracranial field potentials (IFPs) from multiple intermediate areas of the ventral stream of the visual cortex in two behaving monkeys engaged in a rapid face categorization task. Using multivariate pattern analysis (MVPA) techniques, we quantified at millisecond precision the face category information conveyed by IFPs in areas of the ventral stream. We further investigate the relationship between the selectivity and latency of individual electrodes as estimated with classical univariate vs. multivariate techniques and conclude on the similarity and differences between the two approaches.

Cognition in the field: comparison of reversal learning performance in captive and wild passerines

Animal cognitive abilities have traditionally been studied in the lab, but studying cognition in nature could provide several benefits including reduced stress and reduced impact on life-history traits. However, it is not yet clear to what extent cognitive abilities can be properly measured in the wild. Here we present the first comparison of the cognitive performance of individuals from the same population, assessed using an identical test, but in contrasting contexts: in the wild vs. in controlled captive conditions. We show that free-ranging great tits (Parus major) perform similarly to deprived, captive birds in a successive spatial reversal-learning task using automated operant devices. In both captive and natural conditions, more than half of birds that contacted the device were able to perform at least one spatial reversal. Moreover, both captive and wild birds showed an improvement of performance over successive reversals, with very similar learning curves observed in both contexts for each reversal. Our results suggest that it is possible to study cognitive abilities of wild animals directly in their natural environment in much the same way that we study captive animals. Such methods open numerous possibilities to study and understand the evolution and ecology of cognition in natural populations.

When does the visual system need to look back

Visual perception, and in particular object recognition, has traditionally been conceived of as a hierarchical process with a dichotomy between feedforward and feedback. Going forward in the ventral stream (V1/V2→V4→PIT→AIT), cell responses gradually become size and position tolerant, as well

Elevation-related difference in serial reversal learning ability in a nonscatter hoarding passerine

Environments characterized by scarce and variable food supply, termed “harsh environments,” have been hypothesized to favor cognitive abilities that aid an animal in finding food, remembering where it is located, or predicting its availability. Most studies of the “harsh environment” hypothesis have found that scatter hoarders from harsher environments have better spatial memory abilities, but few studies have looked at this hypothesis in nonscatter hoarders. Here, we present the first comparison of performance on a serial reversal learning task in a nonscatter hoarder from 2 elevations that differ in harshness. Serial reversal learning tasks measure a suite of cognitive abilities that are believed to allow an animal to adjust its foraging behavior to match changes in the availability of food over time. Therefore, performance on this task is predicted to increase with elevation. There was no significant difference between the high and low elevation great tits in initial reversal learning accuracy. While both high and low elevation birds were able to improve their reversal learning accuracy, they did not differ in their rate of improvement over reversals. However, we found that lower elevation birds had higher accuracy across all reversals. Contrary to the “harsh environment” hypothesis, our findings suggest that birds from the less harsh environment at low elevation performed more accurately on the reversal learning task. Overall, our results suggest that the study of the relationship between harshness and cognition in nonhoarders would benefit from taking into account other environmental factors, and trade-offs with other cognitive abilities.