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Predisposed mechanisms for social orienting: A comparative neuro-cognitive approach

Final Report Summary - PREMESOR (Predisposed mechanisms for social orienting: A comparative neuro-cognitive approach)

The perceptual world that we experience is full with a variety of objects. The first and most effective way to make sense of it is to identify and differentiate animate entities from inanimate things. Indeed, recognizing and attending to animacy constitutes a crucial step in building up a «social brain», and it has been suggested that lack of this ability may contribute to autism spectrum disorders.
Investigation of the neural and genetic bases of animacy recognition would require a biological approach, with a suitable animal model that may provide a useful comparison with human newborns. The aim of our project was to develop a detailed animal model of vertebrate social predispositions using the domestic chick (Gallus gallus), closely relating this work to equivalent behavioural and neural measures in human neonates, including those at risk of autism, for which there is no widely accepted animal model.
Naïve chicks approach animate creatures, preferring a stuffed jungle fowl to an artificial red box or to a texture-matched box. The role of specific perceptual properties was revealed by testing similar predispositions with more controlled stimuli (schematic faces, semi-rigid or self-propelled motion), which are preferred also by human newborns, suggesting conserved mechanisms. Immediate early genes (IEGs) are rapidly activated after an increase of neuronal activity, with an important role in neuronal plasticity and learning in mammals and birds. Using immediate early genes (IEGs) expression, genes that are rapidly activated after an increase of neuronal activity expression, we found evidence for specific activity associated with innate predispositions to animacy. In our experiments chicks could for example see at the opposite ends of a runway a rotating stuffed jungle fowl and a rotating scrambled jungle fowl (a box, which surface was covered with small pieces of the pelt of a second jungle fowl, attached in random order). These two stimuli were balanced for low-level visual properties such as luminance, colour, visual texture and movement, but they differed in the spatial configuration of the local features that characterise the canonical fowl head. Chicks were free to move in the corridor, during which we recorded if they chose to approach the canonical fowl or the texture-fowl. By using the immediate early gene product c-Fos, we compared neuronal activity in the chicks that approached either one or the other stimulus. We were able to observe for the first time upregulated c-Fos immunoreactive neurons in some specific brain structures, in particular in the lateral septum and in homologous of amigdaloid nuclei. Using simplified computer-generated stimuli that provided only dynamic cues to animacy such as self-propulsion or speed changes we were able to disentangle a specific role of the septum for dynamic stimuli of animacy and of amygdaloid nuclei for static cues of animacy. This selectivity was also lateralized, mainly to the right hemisphere, both in behaviour and in c-fos immunoreactivity. RNA seq analyses further revealed the involvement of specific genes (including those of Nodal cascade) associated with light stimulation in embryo and cerebral hemisphere.
Finally, using the same stimuli that reveal sensitivity and predisposition to attend to animate objects in young chicks, we found that human neonates show sensitivity to exactly the same cues (e.g. self-propulsion, acceleration). EEG and fNIRS recording revealed for the first time specific neural signatures of response to these animacy cues in neonates. Moreover, results with newborns at high familial risk for autism (who have an older sibling diagnosed with autism spectrum disorders) suggest an endophenotype with massive differences in sensitivity to animacy cues between newborns at high-risk of autism and controls. The results revealed early behavioural characteristics of newborns with familial risk for autism spectrum disorders, allowing for a prospective approach to the emergence of autism in early infancy.