An ever-increasing number of functional magnetic resonance imaging (fMRI) studies are now using information-based multi-voxel pattern analysis (MVPA) techniques to decode mental states. In doing so, they achieve a significantly greater sensitivity compared to when they use univariate frameworks. However, the new brain-decoding methods have also posed new challenges for analysis and statistical inference on the group level. We discuss why the usual procedure of performing t-tests on accuracy maps across subjects in order to produce a group statistic is inappropriate. We propose a solution to this problem for local MVPA approaches, which achieves higher sensitivity than other procedures. Our method uses random permutation tests on the single-subject level, and then combines the results on the group level with a bootstrap method. To preserve the spatial dependency induced by local MVPA methods, we generate a random permutation set and keep it fixed across all locations. This enables us to later apply a cluster size control for the multiple testing problem. More specifically, we explicitly compute the distribution of cluster sizes and use this to determine the p-values for each cluster. Using a volumetric searchlight decoding procedure, we demonstrate the validity and sensitivity of our approach using both simulated and real fMRI data sets. In comparison to the standard t-test procedure implemented in SPM8, our results showed a higher sensitivity. We discuss the theoretical applicability and the practical advantages of our approach, and outline its generalization to other local MVPA methods, such as surface decoding techniques.

Statistical inference and multiple testing correction in classification-based multi-voxel pattern analysis (MVPA): random permutations and cluster size control

Do you see what I see

Canis familiaris As a Model for Non-Invasive Comparative Neuroscience.

Objects constitute the fundamental currency of our consciousness: they are the things that we perceive, remember and think about. One of the most important objects for a primate is a face. Research on the macaque face patch system in recent years has given us a remarkable window into the detailed processes underlying object recognition. Here, we review the macaque face patch system, including its anatomical organization, coding principles, role in behaviour and interactions with other brain regions. We highlight not only how it constitutes an archetypal object recognition system but also how it may provide a key to understanding mechanisms for higher cognitive function.

The macaque face patch system: a turtle’s underbelly for the brain

Dogs are hypersocial with humans, and their integration into human social ecology makes dogs a unique model for studying cross-species social bonding. However, the proximal neural mechanisms driving dog-human social interaction are unknown. We used functional magnetic resonance imaging in 15 awake dogs to probe the neural basis for their preferences for social interaction and food reward. In a first experiment, we used the ventral caudate as a measure of intrinsic reward value and compared activation to conditioned stimuli that predicted food, praise or nothing. Relative to the control stimulus, the caudate was significantly more active to the reward-predicting stimuli and showed roughly equal or greater activation to praise vs food in 13 of 15 dogs. To confirm that these differences were driven by the intrinsic value of social praise, we performed a second imaging experiment in which the praise was withheld on a subset of trials. The difference in caudate activation to the receipt of praise, relative to its withholding, was strongly correlated with the differential activation to the conditioned stimuli in the first experiment. In a third experiment, we performed an out-of-scanner choice task in which the dog repeatedly selected food or owner in a Y-maze. The relative caudate activation to food- and praise-predicting stimuli in Experiment 1 was a strong predictor of each dog's sequence of choices in the Y-maze. Analogous to similar neuroimaging studies of individual differences in human social reward, our findings demonstrate a neural mechanism for preference in domestic dogs that is stable within, but variable between, individuals. Moreover, the individual differences in the caudate responses indicate the potentially higher value of social than food reward for some dogs and may help to explain the apparent efficacy of social interaction in dog training.

/pdf/awake-canine-fmri-predicts-dogs-preference-for-praise-vs-1kdm8bxo5t.pdf

Awake canine fMRI predicts dogs' preference for praise vs food.

Dogs have a rich social relationship with humans. One fundamental aspect of it is how dogs pay close attention to human faces in order to guide their behavior, for example, by recognizing their owner and his/her emotional state using visual cues. It is well known that humans have specific brain regions for the processing of other human faces, yet it is unclear how dogs' brains process human faces. For this reason, our study focuses on describing the brain correlates of perception of human faces in dogs using functional magnetic resonance imaging (fMRI). We trained seven domestic dogs to remain awake, still and unrestrained inside an MRI scanner. We used a visual stimulation paradigm with block design to compare activity elicited by human faces against everyday objects. Brain activity related to the perception of faces changed significantly in several brain regions, but mainly in the bilateral temporal cortex. The opposite contrast (i.e., everyday objects against human faces) showed no significant brain activity change. The temporal cortex is part of the ventral visual pathway, and our results are consistent with reports in other species like primates and sheep, that suggest a high degree of evolutionary conservation of this pathway for face processing. This study introduces the temporal cortex as candidate to process human faces, a pillar of social cognition in dogs.

/pdf/our-faces-in-the-dog-s-brain-functional-imaging-reveals-1v9noi1ou3.pdf

Our Faces in the Dog's Brain: Functional Imaging Reveals Temporal Cortex Activation during Perception of Human Faces.

Conspecific-preference in social perception is evident for multiple sensory modalities and in many species. There is also a dedicated neural network for face processing in primates. However, the evolutionary origin and the relative role of neural species sensitivity and face sensitivity in visuo-social processing are largely unknown. In this comparative study, species sensitivity and face sensitivity to identical visual stimuli (videos of human and dog faces and occiputs) were examined using functional magnetic resonance imaging in dogs (n = 20; 45% female) and humans (n = 30; 50% female). In dogs, the bilateral mid suprasylvian gyrus showed conspecific-preference, no regions exhibited face-preference, and the majority of the visually-responsive cortex showed greater conspecific-preference than face-preference. In humans, conspecific-preferring regions (the right amygdala/hippocampus and the posterior superior temporal sulcus) also showed face-preference, and much of the visually-responsive cortex showed greater face-preference than conspecific-preference. Multivariate pattern analyses (MVPAs) identified species-sensitive regions in both species, but face-sensitive regions only in humans. Across-species representational similarity analyses (RSAs) revealed stronger correspondence between dog and human response patterns for distinguishing conspecific from heterospecific faces than other contrasts. Results unveil functional analogies in dog and human visuo-social processing of conspecificity but suggest that cortical specialization for face perception may not be ubiquitous across mammals.SIGNIFICANCE STATEMENT To explore the evolutionary origins of human face-preference and its relationship to conspecific-preference, we conducted the first comparative and noninvasive visual neuroimaging study of a non-primate and a primate species, dogs and humans. Conspecific-preferring brain regions were observed in both species, but face-preferring brain regions were observed only in humans. In dogs, an overwhelming majority of visually-responsive cortex exhibited greater conspecific-preference than face-preference, whereas in humans, much of the visually-responsive cortex showed greater face-preference than conspecific-preference. Together, these findings unveil functional analogies and differences in the organizing principles of visuo-social processing across two phylogenetically distant mammal species.

https://www.jneurosci.org/content/jneuro/40/43/8396.full.pdf

Comparative Brain Imaging Reveals Analogous and Divergent Patterns of Species and Face Sensitivity in Humans and Dogs.

Tactile object categories can be decoded from the parietal and lateral-occipital cortices.

Dogs can interpret emotional human faces (especially the ones expressing happiness), yet the cerebral correlates of this process are unknown. Using functional magnetic resonance imaging (fMRI) we studied eight awake and unrestrained dogs. In Experiment 1 dogs observed happy and neutral human faces, and found increased brain activity when viewing happy human faces in temporal cortex and caudate. In Experiment 2 the dogs were presented with human faces expressing happiness, anger, fear, or sadness. Using the resulting cluster from Experiment 1 we trained a linear support vector machine classifier to discriminate between pairs of emotions and found that it could only discriminate between happiness and the other emotions. Finally, evaluation of the whole-brain fMRI time courses through a similar classifier allowed us to predict the emotion being observed by the dogs. Our results show that human emotions are specifically represented in dogs9 brains, highlighting their importance for inter-species communication.

/pdf/decoding-human-emotional-faces-in-the-dog-s-brain-41407f32h7.pdf

Decoding Human Emotional Faces in the Dog's Brain

Dogs use emotional cues from humans to guide their behavior. Happiness is a basic emotion that humans express and dogs can perceive and interpret. Here, we describe the brain correlates of perception of happy human faces in dogs by using functional magnetic resonance imaging (fMRI). Eight dogs participated: they were trained to remain awake, still, and unrestrained inside an MRI scanner. The visual paradigm included blocks of happy or neutral human faces, with gender matched to each dog's main caretaker. We found brain activity related to happy human faces mainly in the temporal cortex (including Sylvian Gyrus, Straight Gyrus, Proreus and Caudate). These results are consistent with studies in humans showing that the superior temporal cortex plays a key role in the perception of emotional faces. We suggest that perception of happy human faces plays a significant role in the attachment between dogs and humans. This is the first study that directly explores the cerebral correlates in dogs of perception of happiness in human faces.

https://www.biorxiv.org/content/biorxiv/early/2017/05/04/134080.full.pdf

Laura V. Cuaya

Papers

Our Faces in the Dog's Brain: Functional Imaging Reveals Temporal Cortex Activation during Perception of Human Faces.

Comparative Brain Imaging Reveals Analogous and Divergent Patterns of Species and Face Sensitivity in Humans and Dogs.

Tactile object categories can be decoded from the parietal and lateral-occipital cortices.

Decoding Human Emotional Faces in the Dog's Brain

Smile at Me! Dogs Activate The Temporal Cortex Towards Smiling Human Faces