Snakes elicit earlier, and monkey faces, later, gamma oscillations in macaque pulvinar neurons.
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ABSTRACT:
SUBMITTER: Le QV
PROVIDER: S-EPMC4744932 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:There is growing evidence from both behavioral and neurophysiological approaches that primates are able to rapidly discriminate visually between snakes and innocuous stimuli. Recent behavioral evidence suggests that primates are also able to discriminate the level of threat posed by snakes, by responding more intensely to a snake model poised to strike than to snake models in coiled or sinusoidal postures (Etting and Isbell 2014). In the present study, we examine the potential for an underlying neurological basis for this ability. Previous research indicated that the pulvinar is highly sensitive to snake images. We thus recorded pulvinar neurons in Japanese macaques (Macaca fuscata) while they viewed photos of snakes in striking and non-striking postures in a delayed non-matching to sample (DNMS) task. Of 821 neurons recorded, 78 visually responsive neurons were tested with the all snake images. We found that pulvinar neurons in the medial and dorsolateral pulvinar responded more strongly to snakes in threat displays poised to strike than snakes in non-threat-displaying postures with no significant difference in response latencies. A multidimensional scaling analysis of the 78 visually responsive neurons indicated that threat-displaying and non-threat-displaying snakes were separated into two different clusters in the first epoch of 50 ms after stimulus onset, suggesting bottom-up visual information processing. These results indicate that pulvinar neurons in primates discriminate between poised to strike from those in non-threat-displaying postures. This neuronal ability likely facilitates behavioral discrimination and has clear adaptive value. Our results are thus consistent with the Snake Detection Theory, which posits that snakes were instrumental in the evolution of primate visual systems.
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Project description:Cognitive functions rely on the coordinated activity of neurons in many brain regions, but the interactions between cortical areas are not yet well understood. Here we investigated whether low-frequency (?) and high-frequency (?) oscillations characterize different directions of information flow in monkey visual cortex. We recorded from all layers of the primary visual cortex (V1) and found that ?-waves are initiated in input layer 4 and propagate to the deep and superficial layers of cortex, whereas ?-waves propagate in the opposite direction. Simultaneous recordings from V1 and downstream area V4 confirmed that ?- and ?-waves propagate in the feedforward and feedback direction, respectively. Microstimulation in V1 elicited ?-oscillations in V4, whereas microstimulation in V4 elicited ?-oscillations in V1, thus providing causal evidence for the opposite propagation of these rhythms. Furthermore, blocking NMDA receptors, thought to be involved in feedback processing, suppressed ? while boosting ?. These results provide new insights into the relation between brain rhythms and cognition.
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Project description:Rhythm processing involves building expectations according to the hierarchical temporal structure of auditory events. Although rhythm processing has been addressed in the context of predictive coding, the properties of the oscillatory response in different cortical areas are still not clear. We explored the oscillatory properties of the neural response to rhythmic incongruence and the cross-frequency coupling between multiple frequencies to further investigate the mechanisms underlying rhythm perception. We designed an experiment to investigate the neural response to rhythmic deviations in which the tone either arrived earlier than expected or the tone in the same metrical position was omitted. These two manipulations modulate the rhythmic structure differently, with the former creating a larger violation of the general structure of the musical stimulus than the latter. Both deviations resulted in an MMN response, whereas only the rhythmic deviant resulted in a subsequent P3a. Rhythmic deviants due to the early occurrence of a tone, but not omission deviants, seemed to elicit a late high gamma response (60-80 Hz) at the end of the P3a over the left frontal region, which, interestingly, correlated with the P3a amplitude over the same region and was also nested in theta oscillations. The timing of the elicited high-frequency gamma oscillations related to rhythmic deviation suggests that it might be related to the update of the predictive neural model, corresponding to the temporal structure of the events in higher-level cortical areas.
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Project description:Snakes and their relationships with humans and other primates have attracted broad attention from multiple fields of study, but not, surprisingly, from neuroscience, despite the involvement of the visual system and strong behavioral and physiological evidence that humans and other primates can detect snakes faster than innocuous objects. Here, we report the existence of neurons in the primate medial and dorsolateral pulvinar that respond selectively to visual images of snakes. Compared with three other categories of stimuli (monkey faces, monkey hands, and geometrical shapes), snakes elicited the strongest, fastest responses, and the responses were not reduced by low spatial filtering. These findings integrate neuroscience with evolutionary biology, anthropology, psychology, herpetology, and primatology by identifying a neurobiological basis for primates' heightened visual sensitivity to snakes, and adding a crucial component to the growing evolutionary perspective that snakes have long shaped our primate lineage.
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Project description:The superior colliculus (SC) and pulvinar are thought to function as a subcortical visual pathway that bypasses the striate cortex and detects fundamental facial information. We previously investigated neuronal responses in the SC and pulvinar of monkeys during a delayed nonmatching-to-sample task, in which the monkeys were required to discriminate among 35 facial photos of five models and other categories of visual stimuli, and reported that population coding by multiple SC and pulvinar neurons well discriminated facial photos from other categories of stimuli (Nguyen et al., 2013, 2014). However, it remains unknown whether population coding could represent multiple types of facial information including facial identity, gender, facial orientation, and gaze direction. In the present study, to investigate population coding of multiple types of facial information by the SC and pulvinar neurons, we reanalyzed the same neuronal responses in the SC and pulvinar; the responses of 112 neurons in the SC and 68 neurons in the pulvinar in serial 50-ms epochs after stimulus onset were reanalyzed with multidimensional scaling (MDS). The results indicated that population coding by neurons in both the SC and pulvinar classified some aspects of facial information, such as face orientation, gender, and identity, of the facial photos in the second epoch (50-100 ms after stimulus onset). The Euclidean distances between all the pairs of stimuli in the MDS spaces in the SC were significantly correlated with those in the pulvinar, which suggested that the SC and pulvinar function as a unit. However, in contrast with the known population coding of face neurons in the temporal cortex, the facial information coding in the SC and pulvinar was coarse and insufficient. In these subcortical areas, identity discrimination was face orientation-dependent and the left and right profiles were not discriminated. Furthermore, gaze direction information was not extracted in the SC and pulvinar. These results suggest that the SC and pulvinar, which comprise the subcortical visual pathway, send coarse and rapid information on faces to the cortical system in a bottom-up process.
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Project description:Highly efficient systems are needed to link perception with action in the context of the highly complex environments in which primates move and interact. Another important component is, nonetheless, needed for action: selection. When one piece of fruit from a branch is being chosen by a monkey, many other pieces are within reach and visible: do the perceptual features of the objects surrounding a target determine interference effects? In humans, reaching to grasp a desired object appears to integrate the motor features of the objects which might become potential targets - a process which seems to be driven by inhibitory attention mechanisms. Here we show that non-human primates use similar mechanisms when carrying out goal-directed actions. The data indicate that the volumetric features of distractors are internally represented, implying that the basic cognitive operations allowing for action selection have deep evolutionary roots.
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Project description:An important aspect of visual object recognition is the ability to perceive object shape. Two basic components of complex shapes are straight and curved contours. A large body of evidence suggests a modular hierarchy for shape representation progressing from simple and complex orientation in early areas V1 and V2, to increasingly complex stages of curvature representation in V4, TEO, and TE. Here, we reinforce and extend the concept of modular representation. Using intrinsic signal optical imaging in Macaque area V4, we find sub-millimeter sized modules for curvature representation that are organized from low to high curvatures as well as domains with complex curvature preference. We propose a possible 'curvature hypercolumn' within V4. In combination with previous studies, we suggest that the key emergent functions at each stage of cortical processing are represented in systematic, modular maps.
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Project description:Spatial attention is discontinuous, sampling behaviorally relevant locations in theta-rhythmic cycles (3-6 Hz). Underlying this rhythmic sampling are intrinsic theta oscillations in frontal and parietal cortices that provide a clocking mechanism for two alternating attentional states that are associated with either engagement at the presently attended location (and enhanced perceptual sensitivity) or disengagement (and diminished perceptual sensitivity). It has remained unclear, however, how these theta-dependent states are coordinated across the large-scale network that directs spatial attention. The pulvinar is a candidate for such coordination, having been previously shown to regulate cortical activity. Here, we examined pulvino-cortical interactions during theta-rhythmic sampling by simultaneously recording from macaque frontal eye fields (FEF), lateral intraparietal area (LIP), and pulvinar. Neural activity propagated from pulvinar to cortex during periods of engagement, and from cortex to pulvinar during periods of disengagement. A rhythmic reweighting of pulvino-cortical interactions thus defines functional dissociations in the attention network.
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Project description:In both monkeys and humans, the observation of actions performed by others activates cortical motor areas. An unresolved question concerns the pathways through which motor areas receive visual information describing motor acts. Using functional magnetic resonance imaging (fMRI), we mapped the macaque brain regions activated during the observation of grasping actions, focusing on the superior temporal sulcus region (STS) and the posterior parietal lobe. Monkeys viewed either videos with only the grasping hand visible or videos with the whole actor visible. Observation of both types of grasping videos activated elongated regions in the depths of both lower and upper banks of STS, as well as parietal areas PFG and anterior intraparietal (AIP). The correlation of fMRI data with connectional data showed that visual action information, encoded in the STS, is forwarded to ventral premotor cortex (F5) along two distinct functional routes. One route connects the upper bank of the STS with area PFG, which projects, in turn, to the premotor area F5c. The other connects the anterior part of the lower bank of the STS with premotor areas F5a/p via AIP. Whereas the first functional route emphasizes the agent and may relay visual information to the parieto-frontal mirror circuit involved in understanding the agent's intentions, the second route emphasizes the object of the action and may aid in understanding motor acts with respect to their immediate goal.
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Project description:IntroductionVisual processing of ecologically relevant stimuli involves a central bias for stimuli demanding detailed processing (e.g., faces), whereas peripheral object processing is based on coarse identification. Fast detection of animal shapes holding a significant phylogenetic value, such as snakes, may benefit from peripheral vision. The amygdala together with the pulvinar and the superior colliculus are implicated in an ongoing debate regarding their role in automatic and deliberate spatial processing of threat signals.MethodsHere we tested twenty healthy participants in an fMRI task, and investigated the role of spatial demands (the main effect of central vs. peripheral vision) in the processing of fear-relevant ecological features. We controlled for stimulus dependence using true or false snakes; snake shapes or snake faces and for task constraints (implicit or explicit). The main idea justifying this double task is that amygdala and superior colliculus are involved in both automatic and controlled processes. Moreover the explicit/implicit instruction in the task with respect to emotion is not necessarily equivalent to explicit vs. implicit in the sense of endogenous vs. exogenous attention, or controlled vs. automatic processes.ResultsWe found that stimulus-driven processing led to increased amygdala responses specifically to true snake shapes presented in the centre or in the peripheral left hemifield (right hemisphere). Importantly, the superior colliculus showed significantly biased and explicit central responses to snake-related stimuli. Moreover, the pulvinar, which also contains foveal representations, also showed strong central responses, extending the results of a recent single cell pulvinar study in monkeys. Similar hemispheric specialization was found across structures: increased amygdala responses occurred to true snake shapes presented to the right hemisphere, with this pattern being closely followed by the superior colliculus and the pulvinar.ConclusionThese results show that subcortical structures containing foveal representations such as the amygdala, pulvinar and superior colliculus play distinct roles in the central and peripheral processing of snake shapes. Our findings suggest multiple phylogenetic fingerprints in the responses of subcortical structures to fear-relevant stimuli.
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