The Impact of Scene Context on Visual Object Recognition: Comparing Humans, Monkeys, and Computational Models.

During natural vision, we rarely see objects in isolation but rather embedded in rich and complex contexts. Understanding how the brain recognizes objects in natural scenes by integrating contextual information remains a key challenge. To elucidate neural mechanisms compatible with human visual processing, we need an animal model that behaves similarly to humans, so that inferred neural mechanisms can provide hypotheses relevant to the human brain. Here we assessed whether rhesus macaques could model human context-driven object recognition by quantifying visual object identification abilities across variations in the amount, quality, and congruency of contextual cues. Behavioral metrics revealed strikingly similar context-dependent patterns between humans and monkeys. However, neural responses in the inferior temporal (IT) cortex of monkeys that were never explicitly trained to discriminate objects in context, as well as current artificial neural network models, could only partially explain this cross-species correspondence. The shared behavioral variance unexplained by context-naive neural data or computational models highlights fundamental knowledge gaps. Our findings demonstrate an intriguing alignment of human and monkey visual object processing that defies full explanation by either brain activity in a key visual region or state-of-the-art models.

Causal manipulation of gaze-following in the macaque temporal cortex.

Gaze-following, the ability to shift one's own attention to places or objects others are looking at, is essential for social interactions. Single unit recordings from the monkey cortex and neuroimaging work on the human and monkey brain suggest that a distinct region in the temporal cortex, the gaze-following patch (GFP), underpins this ability. Since previous studies of the GFP have relied on correlational techniques, it remains unclear whether gaze-following related activity in the GFP indicates a causal role rather than being just a reverberation of behaviorally relevant information produced elsewhere. To answer this question, we applied focal electrical and pharmacological perturbation to the GFP. Both approaches, when applied to the GFP, disrupted gaze-following if the monkeys had been instructed to follow gaze, along with the ability to suppress it if vetoed by the context. Hence the GFP is necessary for gaze-following as well as its cognitive control.

Long-Term Recording of Subthalamic Aperiodic Activities and Beta Bursts in Parkinson's Disease.

BACKGROUND: Local field potentials (LFPs) represent the summation of periodic (oscillations) and aperiodic (fractal) signals. Although previous studies showed changes in beta band oscillations and burst characteristics of the subthalamic nucleus (STN) in Parkinson's disease (PD), how aperiodic activity in the STN is related to PD pathophysiology is unknown. OBJECTIVES: The study aimed to characterize the long-term effects of STN-deep brain stimulation (DBS) and dopaminergic medications on aperiodic activities and beta bursts. METHODS: A total of 10 patients with PD participated in this longitudinal study. Simultaneous bilateral STN-LFP recordings were conducted in six separate visits during a period of 18 months using the Activa PC + S device in the off and on dopaminergic medication states. We used irregular-resampling auto-spectral analysis to separate oscillations and aperiodic components (exponent and offset) in the power spectrum of STN-LFP signals in beta band. RESULTS: Our results revealed a systematic increase in both the exponent and the offset of the aperiodic spectrum over 18 months following the DBS implantation, independent of the dopaminergic medication state of patients with PD. In contrast, beta burst durations and amplitudes were stable over time and were suppressed by dopaminergic medications. CONCLUSIONS: These findings indicate that oscillations and aperiodic activities reflect at least partially distinct yet complementary neural mechanisms, which should be considered in the design of robust biomarkers to optimize adaptive DBS. Given the link between increased gamma-aminobutyric acidergic (GABAergic) transmission and higher aperiodic activity, our findings suggest that long-term STN-DBS may relate to increased inhibition in the basal ganglia. © 2022 International Parkinson and Movement Disorder Society.

Oculomotor system can differentially process red and green colors during saccade programming in the presence of a competing distractor.

Selective attention filters irrelevant information entering our brain to allow for fine-tuning of the relevant information processing. In the visual domain, shifts of attention are most often followed by a saccadic eye movement to objects and places of high relevance. Recent studies have shown that the stimulus color can affect saccade target selection and saccade trajectories. While those saccade modulations are based on perceptual color space, the level in the visual processing hierarchy at which color selection biases saccade programming remains unclear. As color has also been shown to influence manual response inhibition which is a key function of the prefrontal cortex, we hypothesized that the effects of color on executive functions would also inherently affect saccade programming. To test this hypothesis, we measured behavioral performance and saccade metrics during a modified saccadic Stroop task which reflects competition between color words ("RED" and "GREEN") and their color at the level of the prefrontal cortex. Our results revealed that the oculomotor system can differentially process red and green colors when planning a saccade in the presence of a competing distractor.

The role of temporal cortex in the control of attention.

Attention is an indispensable component of active vision. Contrary to the widely accepted notion that temporal cortex processing primarily focusses on passive object recognition, a series of very recent studies emphasize the role of temporal cortex structures, specifically the superior temporal sulcus (STS) and inferotemporal (IT) cortex, in guiding attention and implementing cognitive programs relevant for behavioral tasks. The goal of this theoretical paper is to advance the hypothesis that the temporal cortex attention network (TAN) entails necessary components to actively participate in attentional control in a flexible task-dependent manner. First, we will briefly discuss the general architecture of the temporal cortex with a focus on the STS and IT cortex of monkeys and their modulation with attention. Then we will review evidence from behavioral and neurophysiological studies that support their guidance of attention in the presence of cognitive control signals. Next, we propose a mechanistic framework for executive control of attention in the temporal cortex. Finally, we summarize the role of temporal cortex in implementing cognitive programs and discuss how they contribute to the dynamic nature of visual attention to ensure flexible behavior.

Variability of neuronal responses in the posterior superior temporal sulcus predicts choice behavior during social interactions.

Recent studies have shown that neural activity in a well-defined patch in the posterior superior temporal sulcus (the "gaze-following patch," GFP) of the primate brain is strongly modulated when the other's gaze attracts the observer's attention to locations/objects, the other is looking at. Changes of the mean discharge rate of neurons in the monkey GFP indicate that they are involved in two distinct computations: the allocation of spatial attention guided by the other's gaze vector and the suppression of gaze following if inappropriate in a given situation. Here, we asked if and how the discharge variability of neurons in the GFP is related to the task and if it carries information on behavioral performance. To this end, we calculated the Fano factor as a measure of across-trial discharge variability as a function of time. Our results show that all neurons exhibiting a task-related discharge-rate modulation also exhibit a stimulus onset-dependent drop in the Fano factor. Furthermore, the amplitude of the Fano factor reduction is modulated by task condition and the neuron's selectivity in this regard. We found that these effects are directly related to the monkeys' behavioral performance in that the Fano factor is predictive about upcoming correct or wrong decisions. Our results indicate that neuronal discharge variability as gauged by the Fano factor, hitherto primarily studied in the context of visual perception or motor control, is an informative measure also in studies of the neural underpinnings of complex social behavior.NEW & NOTEWORTHY Quenching of neural variability following stimulus onset is a widely accepted phenomenon. However, the relevance of quenching for the shaping of complex social behaviors remains to be explored. Here, we show that task selective neurons in the GFP exhibit a higher degree of variability quenching than their neighboring unselective neurons. Furthermore, we demonstrate that behavioral errors are not only associated with lower firing rates but also less variability quenching, suggesting that both facilitate optimal performance.

V1 neurons encode the perceptual compensation of false torsion arising from Listing's law.

We try to deploy the retinal fovea to optimally scrutinize an object of interest by directing our eyes to it. The horizontal and vertical components of eye positions acquired by goal-directed saccades are determined by the object's location. However, the eccentric eye positions also involve a torsional component, which according to Donder's law is fully determined by the two-dimensional (2D) eye position acquired. According to von Helmholtz, knowledge of the amount of torsion provided by Listing's law, an extension of Donder's law, alleviates the perceptual interpretation of the image tilt that changes with 2D eye position, a view supported by psychophysical experiments he pioneered. We address the question of where and how Listing's law is implemented in the visual system and we show that neurons in monkey area V1 use knowledge of eye torsion to compensate the image tilt associated with specific eye positions as set by Listing's law.

Decoding of the other's focus of attention by a temporal cortex module.

Faces attract the observer's attention toward objects and locations of interest for the other, thereby allowing the two agents to establish joint attention. Previous work has delineated a network of cortical "patches" in the macaque cortex, processing faces, eventually also extracting information on the other's gaze direction. Yet, the neural mechanism that links information on gaze direction, guiding the observer's attention to the relevant object, has remained elusive. Here we present electrophysiological evidence for the existence of a distinct "gaze-following patch" (GFP) with neurons that establish this linkage in a highly flexible manner. The other's gaze and the object, singled out by the gaze, are linked only if this linkage is pertinent within the prevailing social context. The properties of these neurons establish the GFP as a key switch in controlling social interactions based on the other's gaze.

Following Eye Gaze Activates a Patch in the Posterior Temporal Cortex That Is not Part of the Human "Face Patch" System.

Humans follow another person's eye gaze to objects of interest to the other, thereby establishing joint attention, a first step toward developing a theory of the other's mind. Previous functional MRI studies agree that a "gaze-following patch" (GFP) of cortex close to the posterior superior temporal sulcus (STS) is specifically implicated in eye gaze-following. The location of the GFP is in the vicinity of the posterior members of the core face-processing system that consists of distinct patches in ventral visual cortex, the STS, and frontal cortex, also involved in processing information on the eyes. To test whether the GFP might correspond to one of the posterior face patches, we compared the pattern of blood oxygenation level-dependent (BOLD) imaging contrasts reflecting the passive vision of static faces with the one evoked by shifts of attention guided by the eye gaze of others. The viewing of static faces revealed the face patch system. On the other hand, eye gaze-following activated a cortical patch (the GFP) with its activation maximum separated by more than 24 mm in the right and 19 mm in the left hemisphere from the nearest face patch, the STS face area (FA). This segregation supports a distinct function of the GFP, different from the elementary processing of facial information.