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Identification of superior colliculus (SC) neurons and the analysis of SC neuronal responses. (A) An example of superimposed traces of a SC neuron. (B) Autocorrelograms of the neurons indicated in (A). Bin width, 1 ms. The ordinate indicates probability where bin counts were divided by the number of spikes in the spike train. (C) A perievent histogram of the neuron indicated in (A), showing responses to a visual stimulus. Bin width, 25 ms. The dashed line indicates the onset of stimulus presentation, and the horizontal bar indicates the duration of the stimulus (500 ms). (D) Magnitudes of the SC neuronal responses indicated in (C). The stimulus duration was divided into 20 epochs (25 ms each). The response magnitudes (spikes/s) were defined as follows: the mean firing rate in each epoch minus the mean firing rate during the 100-ms period before stimulus onset.
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The superficial layers of the superior colliculus (sSC) appear to function as a subcortical visual pathway that bypasses the striate cortex for the rapid processing of coarse facial information. We investigated the responses of neurons in the monkey sSC during a delayed non-matching-to-sample (DNMS) task in which monkeys were required to discrimina...
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The EU-Emotion Stimulus Set is a newly developed collection of dynamic multimodal emotion and mental state representations. A total of 20 emotions and mental states are represented through facial expressions, vocal expressions, body gestures and contextual social scenes. This emotion set is portrayed by a multi-ethnic group of child and adult actor...
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... Recent work has expanded the understanding of the brainstem feature-detection system by showing that evolutionarily-relevant stimuli, like faces and snakes, evoke shorter latency orientation movements than other kinds of visual stimuli (Almeida et al., 2015;Bannerman et al., 2009Bannerman et al., , 2010Martin et al., 2018) . In addition, neurons in the primate SC and pulvinar exhibit lower latencies (~50ms) and larger bursts in response to faces than other visual stimuli (Almeida et al., 2015;Nguyen et al., 2013Nguyen et al., , 2014Nguyen et al., , 2016Yu et al., 2023) . These subcortical networks are thought to play a crucial role in the detection of faces and facial expressions in patients with lesions of the primary visual cortex (Celeghin et al., 2019) . ...
... The use of geometric shapes in experiment 2 allows us to control for spatial frequency and luminance without reduction in image clarity. High contrast images of this type have been found to elicit higher neural activity in the SC of the monkey when compared to natural images of faces (Nguyen et al., 2013(Nguyen et al., , 2014(Nguyen et al., , 2016Van Le et al., 2020) . ...
... Recordings in the primate SC show that presentation of face or face-like stimuli can influence the vigor of visual responses within <50ms (Almeida et al., 2015;Nguyen et al., 2014Nguyen et al., , 2016Yu et al., 2023) . Given that the tecto-reticulo-spinal pathway is hypothesized to mediate the EVR on the upper limb (Corneil & Munoz, 2014;Pruszynski et al., 2010) , we investigated if presentation of face or face-like stimuli influence the magnitude of the EVR. ...
The superior colliculus (SC) has been increasingly implicated in the rapid processing of evolutionarily relevant visual stimuli like faces, but the behavioural relevance of such processing is not clear. The SC has also been implicated in the generation of upper-limb Express Visuomotor Responses (EVRs) on upper limb muscles, which are very short-latency (within ∼80 ms) bursts of muscle activity time-locked to visual target presentation. This reasoning led us to investigate the influence of faces on EVRs.
We recorded upper limb muscle activity from young healthy participants as they reached toward left or right targets in the presence of a distractor stimulus presented on the opposite side. Across blocks of trials, we varied the instruction as to which stimulus served as the target or distractor. Doing so allowed us to assess the impact of instruction on muscle recruitment by examining trials when the exact same stimuli required a reach to either the left or right. We found that EVRs were uniquely modulated in tasks involving face selection, promoting reaches toward or away from faces depending on instruction. Follow-up experiments confirmed that this phenomenon required highly salient repeated faces, and was not observed to non-facial salient stimuli nor to faces expressing different affect. We conclude that our results attest to an integration of top-down task set and bottom-up feature detection to promote rapid motor responses to faces at latencies that match or precede the arrival of face information in human cortex.
STATEMENT OF SIGNIFICANCE
The tecto-reticulo-spinal pathway is hypothesized to mediate the express visuomotor response (EVR). This study extends this hypothesis by demonstrating that face detection in the subcortex impacts low-latency movement via the EVR at latencies preceding cortical activity for face perception. To date, this constitutes the most direct evidence for direct behavioural relevance of rapid face detection in the brainstem. Further, we find that this response can be modulated by task context, allowing for different instruction-based responses given the exact same visual stimulus and implicating top-down cortical control of the EVR.
... Indeed, in 1974, Updyke 9 observed neurons in the superior colliculus (SC), a site of convergence for retinal and extra-retinal visual signals 10 , that were particularly sensitive to three-dimensional objects, and SC cells sensitive to complex visual stimuli were also reported by Rizzolatti and colleagues in 1980 11 . More recently, a series of seminal studies explored the roles of the SC and pulvinar in the processing of face and snake images [12][13][14][15][16][17][18] . These studies concluded that the SC may be part of a fast detection network for visual threats and ecologically-relevant faces, which can in turn influence emotions 6 . ...
... Because we ran only one exemplar from each object category in a given session, it was not easy to convincingly assess whether SC neurons also exhibit early object recognition capabilities, besides detecting extrafoveal objects. Future experiments could investigate this possibility in more detail, as in, for example, the studies investigating SC face preference [15][16][17][18][19] . ...
Primate superior colliculus (SC) neurons exhibit visual feature tuning properties and are implicated in a subcortical network hypothesized to mediate fast threat and/or conspecific detection. However, the mechanisms through which SC neurons contribute to peripheral object detection, for supporting rapid orienting responses, remain unclear. Here we explored whether, and how quickly, SC neurons detect real-life object stimuli. We presented experimentally-controlled gray-scale images of seven different object categories, and their corresponding luminance- and spectral-matched image controls, within the extrafoveal response fields of SC neurons. We found that all of our functionally-identified SC neuron types preferentially detected real-life objects even in their very first stimulus-evoked visual bursts. Intriguingly, even visually-responsive motor-related neurons exhibited such robust early object detection. We further identified spatial frequency information in visual images as an important, but not exhaustive, source for the earliest (within 100 ms) but not for the late (after 100 ms) component of object detection by SC neurons. Our results demonstrate rapid and robust detection of extrafoveal visual objects by the SC. Besides supporting recent evidence that even SC saccade-related motor bursts can preferentially represent visual objects, these results reveal a plausible mechanism through which rapid orienting responses to extrafoveal visual objects can be mediated.
... Frontiers in Systems Neuroscience 04 frontiersin.org viewing paradigms circumvents this issue and has indeed revealed several seemingly inherent feature sensitivities in the intermediate (visuomotor) layers of SC: orientation (Chen and Hafed, 2018), spatial frequency (Chen and Hafed, 2017), color (White et al., 2009), motion direction (Davidson and Bender, 1991;Horwitz and Newsome, 2001), and face detection (Nguyen et al., 2014;Le et al., 2020). Similarly, a classic study of FEF visual response properties found that 12% of purely visual FEF neurons show featural sensitivity for color and motion (Mohler et al., 1973), while more recent studies have found that between 31 and 54% of visuomotor FEF neurons exhibit sensitivity for motion direction and speed (Barborica and Ferrera, 2003;Xiao et al., 2006). ...
Eye movements are often directed toward stimuli with specific features. Decades of neurophysiological research has determined that this behavior is subserved by a feature-reweighting of the neural activation encoding potential eye movements. Despite the considerable body of research examining feature-based target selection, no comprehensive theoretical account of the feature-reweighting mechanism has yet been proposed. Given that such a theory is fundamental to our understanding of the nature of oculomotor processing, we propose an oculomotor feature-reweighting mechanism here. We first summarize the considerable anatomical and functional evidence suggesting that oculomotor substrates that encode potential eye movements rely on the visual cortices for feature information. Next, we highlight the results from our recent behavioral experiments demonstrating that feature information manifests in the oculomotor system in order of featural complexity, regardless of whether the feature information is task-relevant. Based on the available evidence, we propose an oculomotor feature-reweighting mechanism whereby (1) visual information is projected into the oculomotor system only after a visual representation manifests in the highest stage of the cortical visual processing hierarchy necessary to represent the relevant features and (2) these dynamically recruited cortical module(s) then perform feature discrimination via shifting neural feature representations, while also maintaining parity between the feature representations in cortical and oculomotor substrates by dynamically reweighting oculomotor vectors. Finally, we discuss how our behavioral experiments may extend to other areas in vision science and its possible clinical applications.
... This second pathway is adaptive to help the body respond quickly to threatening stimuli (Terburg et al., 2018). In an electrophysiological study, with single-cell recordings in monkeys, researchers found that the superior colliculus was able to rapidly process facial information before sending information along to the pulvinar (Nguyen et al., 2014). Evidence is further amounting for the existence of this same route in humans (Diano et al., 2017;Garvert et al., 2014;Rafal et al., 2015), and damage in this route interferes with responses to visual threats in the environment (Bertini et al., 2018;Ward et al., 2005). ...
While emotions, thoughts, and behaviors are considered to each impact one another, cognitive interventions have come to dominate most forms of psychotherapy practiced today. This assumes the cognitive primacy hypothesis, which is often considered to be in opposition to the affective primacy hypothesis. These two hypotheses are examined in conjunction with recent advances in psychological research along with the neuroscience of evaluative processing models. Research is investigated to determine if cognitive models like the A–B–C model are the most applicable to psychotherapy. Research does not find support for either the cognitive or affective primacy hypotheses. Neuroscience research indicates that cognition and emotion interact dynamically, unlike previously proposed linear models of therapeutic change (A–B–C model, insight for therapeutic change). Given such, emotional interventions in psychotherapy should be applied in tandem with cognitive interventions. Emotional interventions should be considered as relevant as cognitive interventions in the practice of psychotherapy, given there is no single linear model starting with cognitive or affective primacy.
... Another example of a biologically relevant contextual stimulus involving numerousness that might be encoded at the subcortical level is a prototypic face-like configuration. Nguyen et al. (2014) recorded neural responses from the monkey superior colliculus to a face-like pattern (three dark dots on a bright oval), representing eyes and the mouth. The neural response to this triangular configuration was different to scrambled images. ...
Perception of numerousness, i.e. number of items in a set, is an important cognitive ability, which is present in several animal taxa. In spite of obvious differences in neuroanatomy, insects, fishes, reptiles, birds, and mammals all possess a "number sense". Furthermore, information regarding numbers can belong to different sensory modalities: animals can estimate a number of visual items, a number of tones, or a number of their own movements. Given both the heterogeneity of stimuli and of the brains processing these stimuli, it is hard to imagine that number cognition can be traced back to the same evolutionary conserved neural pathway. However, neurons that selectively respond to the number of stimuli have been described in higher-order integration brain centres both in primates and in birds, two evolutionary distant groups. Although most probably not of the same evolutionary origin, these number neurons share remarkable similarities in their response properties. Instead of homology, this similarity might result from computational advantages of the underlying coding mechanism. This means that one might expect numerousness information to undergo similar steps of neural processing even in evolutionary distant neural pathways. Following this logic, in this review we summarize our current knowledge of how numerousness is processed in the brain from sensory input to coding of abstract information in the higher-order integration centres. We also propose a list of key open questions that might promote future research on number cognition.
... This suggests that the SC might have access to mechanisms associated with the perception of high-level visual forms. More recently, SC responses to faces and face-like stimuli were reported (Le et al. 2020, Nguyen et al. 2014, Soares et al. 2017, and it was suggested that these responses are early enough to allow the SC to act as a fast object detector. Indeed, tests exploring the influences of task-irrelevant visual forms on target selection for saccades and manual responses revealed that there was an express influence of visual forms, versus scrambled but spectrally equivalent visual scenes, on reaction times (Bogadhi et al. 2020). ...
The superior colliculus (SC) is a subcortical brain structure that is relevant for sensation, cognition, and action. In nonhuman primates, a rich history of studies has provided unprecedented detail about this structure's role in controlling orienting behaviors; as a result, the primate SC has become primarily regarded as a motor control structure. However, as in other species, the primate SC is also a highly visual structure: A fraction of its inputs is retinal and complemented by inputs from visual cortical areas, including the primary visual cortex. Motivated by this, recent investigations are revealing the rich visual pattern analysis capabilities of the primate SC, placing this structure in an ideal position to guide orienting movements. The anatomical proximity of the primate SC to both early visual inputs and final motor control apparatuses, as well as its ascending feedback projections to the cortex, affirm an important role for this structure in active perception.
Expected final online publication date for the Annual Review of Vision Science, Volume 9 is September 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
... Such faster rise to the decision threshold in our study, could be a consequence of a shortcut pathway, most likely through subcortical areas such as the amygdala or superior colliculus, being able to interpret other's gaze direction to shift spatial attention, ultimately speeding up saccadic target selection. There are several experiments on monkeys supporting the existence of such a pathway and its sensitivity to facial information (Nguyen et al., 2014;Taubert et al., 2018). This notion gets further support from psychophysical experiments in monkeys using other behavioural paradigms more sensitive to capture temporal aspects of gaze following (Marciniak et al., 2015), which suggest that the early component of gaze following cannot be fully suppressed in response to cognitive control signals. ...
Gaze following is a major element of non-verbal communication and important for successful social interactions. Human gaze following is a fast and almost reflex-like behavior, yet, it can be volitionally controlled and suppressed to some extent if inappropriate or unnecessary, given the social context. In order to identify the neural basis of the cognitive control of gaze following, we carried out an event-related fMRI experiment, in which human subjects' eye movements were tracked while they were exposed to gaze cues in two distinct contexts: a baseline gaze following condition in which subjects were instructed to use gaze cues to shift their attention to a gazed-at spatial target and a control condition in which the subjects were required to ignore the gaze cue and instead to shift their attention to a distinct spatial target to be selected based on a color mapping rule, requiring the suppression of gaze following. We could identify a suppression-related BOLD response in a frontoparietal network comprising dorsolateral prefrontal cortex (dlPFC), orbitofrontal cortex (OFC), the anterior insula, precuneus and posterior parietal cortex (PPC). These findings suggest that over excitation of frontoparietal circuits in turn suppressing the gaze following patch might be a potential cause of gaze following deficits in clinical populations.
... However, pulvinar neural responses to snakes could well reflect visual information from the dense projections from medial and inferotemporal (IT) cortices, characterizing a brain region homologous with the fusiform face area in humans, where cortical face processing occurs along with unrelated shapes in macaque IT (Benevento and Miller, 1981;Tanaka, 2003). Therefore, the pattern recognition capabilities by the primate SC are ambiguous, beyond that of rough face perception with two facing eyes (Nguyen et al., 2014) that is much more evolutionarily refined in the human fusiform face area and occipital face area (cf. Arcurio et al., 2012;Cecchini et al., 2013;Parkington and Itier, 2018). ...
This is a collection of 21 articles published as an eBook in Frontiers in Psychology. This Research Topic aims to demonstrate that imaginative culture is an important functional part of evolved human behavior—diverse in its manifestations but unified by species-typical sets of biologically grounded motives, emotions, and cognitive dispositions. The topic encompasses four main areas of research in the evolutionary human sciences: (1) evolutionary psychology and anthropology, which have fashioned a robust model of evolved human motives organized systemically within the phases and relationships of human life history; (2) research on gene-culture coevolution, which has illuminated the mechanisms of social cognition and the transmission of cultural information; (3) the psychology of emotions and affective neuroscience, which have gained precise knowledge about the evolutionary basis and neurological character of the evolved emotions that give power to the arts, religion, and ideology; and (4) cognitive neuroscience, which has identified the Default Mode Network as the central neurological location of the human imagination. By integrating these four areas of research and by demonstrating their value in illuminating specific kinds of imaginative culture, this Research Topic aims at incorporating imaginative culture within an evolutionary conception of human nature.
... First, response selectivity in the SC to face-like patterns or to stimuli evolutionary relevant for survival (e.g. prey, predators, food) occurs as early as 50 ms after the stimulus onset [23][24][25]. For comparison, the human amygdala's shortest responses to facial expressions have been reported at about 70 ms, while emotional modulation of V1/V2 activity peaks at 80 ms [26]. ...
Although sensory processing is pivotal to nearly every theory of emotion, the evaluation of the visual input as 'emotional' (e.g. a smile as signalling happiness) has been traditionally assumed to take place in supramodal 'limbic' brain regions. Accordingly, subcortical structures of ancient evolutionary origin that receive direct input from the retina, such as the superior colliculus (SC), are traditionally conceptualized as passive relay centres. However, mounting evidence suggests that the SC is endowed with the necessary infrastructure and computational capabilities for the innate recognition and initial categorization of emotionally salient features from retinal information. Here, we built a neurobiologically inspired convolutional deep neural network (DNN) model that approximates physiological, anatomical and connectional properties of the retino-collicular circuit. This enabled us to characterize and isolate the initial computations and discriminations that the DNN model of the SC can perform on facial expressions, based uniquely on the information it directly receives from the virtual retina. Trained to discriminate facial expressions of basic emotions, our model matches human error patterns and above chance, yet suboptimal, classification accuracy analogous to that reported in patients with V1 damage, who rely on retino-collicular pathways for non-conscious vision of emotional attributes. When presented with gratings of different spatial frequencies and orientations never 'seen' before, the SC model exhibits spontaneous tuning to low spatial frequencies and reduced orientation discrimination, as can be expected from the prevalence of the magnocellular (M) over parvocellular (P) projections. Likewise, face manipulation that biases processing towards the M or P pathway affects expression recognition in the SC model accordingly, an effect that dovetails with variations of activity in the human SC purposely measured with ultra-high field functional magnetic resonance imaging. Lastly, the DNN generates saliency maps and extracts visual features, demonstrating that certain face parts, like the mouth or the eyes, provide higher discriminative information than other parts as a function of emotional expressions like happiness and sadness. The present findings support the contention that the SC possesses the necessary infrastructure to analyse the visual features that define facial emotional stimuli also without additional processing stages in the visual cortex or in 'limbic' areas. This article is part of the theme issue 'Cracking the laugh code: laughter through the lens of biology, psychology and neuroscience'.
... This may be responsible for the lack of eyespot recognition as seen from the lack of discrimination between our control and the two circles. In humans and other mammals, the superior colliculus is responsible for the detection and response to face-like stimuli, including eye-like patterns (Nguyen et al., 2013(Nguyen et al., , 2014Reid et al., 2017). The optic tectum is the primary visual center for lizard visual perception which parallels the mammalian superior colliculus (Stein et al., 1976). ...
The extent to which prey respond to predation risk may depend upon the level of threat it perceives. A prey's perception of a threat can also be influenced by the background levels of predatory threat in the environment. Many animals also rely on visual cues to discriminate threat and assess risk. Eyes, in particular, are known to elicit an aversive response in prey. However, there is a lack of the literature about what salient physical features of a predator's gaze triggers aversion in prey, especially reptilian prey. We capitalized on the putatively aversive effects of eyes to better understand the influence of average background threat on risk perception. We approached blue-tailed skinks (Emoia impar) with four different treatments: a blank control and three experimental treatments (two circular eyes, two squares, and one big circle) to test whether eye shape or number induced a greater aversive response in prey measured by the time allocated to key activities, as well as by flight initiation distance (FID) in locations of high and low background threat. Skinks discriminated more between treatments at low risk than in high risk situations by varying their behavior in response to treatments only in low-risk scenarios, but this did not translate into differences in FID. Our results suggest that in high-risk situations, the cost to discriminate is higher than at low risk. Although we can assume our treatments were not perceived as eyes due to a lack of discrimination toward the two circle treatment, detectability and more specifically diameter of stimuli are the most salient to skinks. While skinks are able to detect subtle differences in visual stimuli, this does not affect their overall fear response. Remarkably, skinks, a species not hunted by humans, have the ability to discriminate subtle features about them, a finding that is seen in other species and requires more study.
