Superior colliculus lesions impair threat responsiveness in infant capuchin monkeys

Maior, Rafael S.; Hori, Etsuro; Barros, Marília; Teixeira, Danilo Simonini; Tavares, Maria Clotilde Henriques; Ono, Taketoshi; Nishijo, Hisao; Tomaz, Carlos

doi:10.1016/j.neulet.2011.09.042

Cited by 55 publications

(45 citation statements)

References 32 publications

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“…Stimulation of its deeper layers causes animals to turn, dart, or freeze (20). Infant monkeys with bilateral neurotoxic lesions of the superior colliculus continue to reach for food in the presence of a snake model, whereas shamoperated monkeys avoid the food (21). Evasive movements such as these are typical of animals that are surprised or threatened by others (22,23).…”

Section: Discussionmentioning

confidence: 99%

Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes

Isbell

Matsumoto

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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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.evolution | Snake Detection Theory | visual responses | low-pass filtered images S nakes have long been of interest to us above and beyond the attention we give to other wild animals. The attributes of snakes and our relationships with them have been topics of discussion in fields as disparate as religion, philosophy, anthropology, psychology, primatology, and herpetology (1, 2). Ochre and eggshells dated to as early as 75,000 y ago and found with cross-hatched and ladder-shaped lines (3, 4) resemble the dorsal and ventral scale patterns of snakes. As the only natural objects with those characteristics, snakes may have been among the first models used in representational imagery created by modern humans. Our interest in snakes may have originated much further back in time; our primate lineage has had a long and complex evolutionary history with snakes as competitors, predators, and prey (1). The position of primates as prey of snakes has, in fact, been argued to have constituted strong selection favoring the evolution of the ability to detect snakes quickly as a means of avoiding them, beginning with the earliest primates (2, 5). Across primate species, ages, and (human) cultures, snakes are indeed detected visually more quickly than innocuous stimuli, even in cluttered scenes (6-11). Physiological responses reveal that humans are also able to detect snakes visually even before becoming consciously aware of them (12). Although the visual system must be involved in the preferential ability to detect snakes rapidly and preconsciously or automatically, the neurological basis for this ability has not yet been elucidated, perhaps because an evolutionary perspective is rarely incorporated in neuroscientific studies. Our study helps to fill this interdisciplinary gap by investigating the responses of neurons to snakes and other natural stimuli that may have acted as selective pressures on primates in the past.Here, we identify a mechanism for the visual system's involvement in rapid snake detection by measurin...

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Section: Discussionmentioning

confidence: 99%

Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes

Isbell

Matsumoto

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

223

157

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“…Evolutionarily old subcortical structures, such as the superior colliculus (SC), for instance, do appear to be sensitive to threat cues (Maior et al 2011). SC (known as the optic tectum in non-mammals) has projections to the koniocellular (K) layers of the lateral geniculate nucleus, and also projects to the pulvinar and mediodorsal nuclei of the thalamus.…”

Section: Social Visual Perceptionmentioning

confidence: 99%

Social Vision: Functional Forecasting and the Integration of Compound Social Cues

Adams

Kveraga

2015

Rev.Phil.Psych.

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For decades the study of social perception was largely compartmentalized by type of social cue: race, gender, emotion, eye gaze, body language, facial expression etc. This was partly due to good scientific practice (e.g., controlling for extraneous variability), and partly due to assumptions that each type of social cue was functionally distinct from others. Herein, we present a functional forecast approach to understanding compound social cue processing that emphasizes the importance of shared social affordances across various cues (see too Adams, Franklin, Nelson, & Stevenson, 2010; Adams & Nelson, 2011; Weisbuch & Adams, 2012). We review the traditional theories of emotion and face processing that argued for dissociable and noninteracting pathways (e.g., for specific emotional expressions, gaze, identity cues), as well as more recent evidence for combinatorial processing of social cues. We argue here that early, and presumably reflexive, visual integration of such cues is necessary for adaptive behavioral responding to others. In support of this claim, we review contemporary work that reveals a flexible visual system, one that readily incorporates meaningful contextual influences in even nonsocial visual processing, thereby establishing the functional and neuroanatomical bases necessary for compound social cue integration. Finally, we explicate three likely mechanisms driving such integration. Together, this work implicates a role for cognitive penetrability in visual perceptual abilities that have often been (and in some cases still are) ascribed to direct encapsulated perceptual processes.

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“…SC is an important and well-known structure related to visual information (for review [22]), however SC also receives multisensory information, such as tactile and auditory [26], [32], [33]. SC deep layers are also related to defensive behaviours such as freezing, darting and shift of attention in rodents [20], [34], [35], as well as prey-predator behaviour in primates [23], [24]. Therefore, further testing might lead to a better understanding of SC's role in nonhuman primate PPI.…”

Section: Discussionmentioning

confidence: 99%

“…The SC-sham group was submitted to the same overall procedure, but instead IBO, the same volume of PBS vehicle was infused. For more details about surgery and evaluation of extent of injury, see Maior et al [23]. We also submitted the same eight animals (control group) cited above to the PPI test described in this session.…”

Section: Methodsmentioning

confidence: 99%

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Whole-Body Prepulse Inhibition Protocol to Test Sensorymotor Gating Mechanisms in Monkeys

et al. 2014

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Prepulse inhibition (PPI) is the decrease of startle reflex amplitude when a slight stimulus is previously generated. This paradigm may provide valuable information about sensorimotor gating functionality. Here we aimed at determining the inhibited and uninhibited startle response of capuchin monkeys (Sapajus spp.), and to evaluate the role of the superior colliculus in PPI. Capuchin monkeys were tested in a whole-body protocol, to determine the best startle amplitude and interstimuli interval. Additionally we tested two subjects with bilateral superior colliculus damage in this protocol. Results show that 115 dB auditory pulse has induced the best startle response. In contrast to reports in other species, no habituation to the auditory stimuli was observed here in capuchins. Also, startle reflex inhibition was optimal after 120 msec interstimuli interval. Finally, there was a downward tendency of percentage inhibition in superior colliculus-lesioned monkeys. Our data provides the possibility of further studies with whole-body protocol in capuchin monkeys and reinforces the importance of the superior colliculus in PPI.

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Superior colliculus lesions impair threat responsiveness in infant capuchin monkeys

Cited by 55 publications

References 32 publications

Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes

Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes

Social Vision: Functional Forecasting and the Integration of Compound Social Cues

Whole-Body Prepulse Inhibition Protocol to Test Sensorymotor Gating Mechanisms in Monkeys

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