Neural evidence for referential understanding of object words in dogs.

Using words to refer to objects in the environment is a core feature of the human language faculty. Referential understanding assumes the formation of mental representations of these words.1,2 Such understanding of object words has not yet been demonstrated as a general capacity in any non-human species,3 despite multiple behavior-based case reports.4,5,6,7,8,9,10 In human event-related potential (ERP) studies, object word knowledge is typically tested using the semantic violation paradigm, where words are presented either with their referent (match) or another object (mismatch).11,12 Such mismatch elicits an N400 effect, a well-established neural correlate of semantic processing.12,13 Reports of preverbal infant N400 evoked by semantic violations14 assert the use of this paradigm to probe mental representations of object words in nonverbal populations. Here, measuring dogs' (Canis familiaris) ERPs to objects primed with matching or mismatching object words, we found a mismatch effect at a frontal electrode, with a latency (206-606 ms) comparable to the human N400. A greater difference for words that dogs knew better, according to owner reports, further supported a semantic interpretation of this effect. Semantic expectations emerged irrespective of vocabulary size, demonstrating the prevalence of referential understanding in dogs. These results provide the first neural evidence for object word knowledge in a non-human animal. VIDEO ABSTRACT.

Speech naturalness detection and language representation in the dog brain.

Family dogs are exposed to a continuous flow of human speech throughout their lives. However, the extent of their abilities in speech perception is unknown. Here, we used functional magnetic resonance imaging (fMRI) to test speech detection and language representation in the dog brain. Dogs (n = 18) listened to natural speech and scrambled speech in a familiar and an unfamiliar language. Speech scrambling distorts auditory regularities specific to speech and to a given language, but keeps spectral voice cues intact. We hypothesized that if dogs can extract auditory regularities of speech, and of a familiar language, then there will be distinct patterns of brain activity for natural speech vs. scrambled speech, and also for familiar vs. unfamiliar language. Using multivoxel pattern analysis (MVPA) we found that bilateral auditory cortical regions represented natural speech and scrambled speech differently; with a better classifier performance in longer-headed dogs in a right auditory region. This neural capacity for speech detection was not based on preferential processing for speech but rather on sensitivity to sound naturalness. Furthermore, in case of natural speech, distinct activity patterns were found for the two languages in the secondary auditory cortex and in the precruciate gyrus; with a greater difference in responses to the familiar and unfamiliar languages in older dogs, indicating a role for the amount of language exposure. No regions represented differently the scrambled versions of the two languages, suggesting that the activity difference between languages in natural speech reflected sensitivity to language-specific regularities rather than to spectral voice cues. These findings suggest that separate cortical regions support speech naturalness detection and language representation in the dog brain.

Neural processes underlying statistical learning for speech segmentation in dogs.

To learn words, humans extract statistical regularities from speech. Multiple species use statistical learning also to process speech, but the neural underpinnings of speech segmentation in non-humans remain largely unknown. Here, we investigated computational and neural markers of speech segmentation in dogs, a phylogenetically distant mammal that efficiently navigates humans' social and linguistic environment. Using electroencephalography (EEG), we compared event-related responses (ERPs) for artificial words previously presented in a continuous speech stream with different distributional statistics. Results revealed an early effect (220-470 ms) of transitional probability and a late component (590-790 ms) modulated by both word frequency and transitional probability. Using fMRI, we searched for brain regions sensitive to statistical regularities in speech. Structured speech elicited lower activity in the basal ganglia, a region involved in sequence learning, and repetition enhancement in the auditory cortex. Speech segmentation in dogs, similar to that of humans, involves complex computations, engaging both domain-general and modality-specific brain areas. VIDEO ABSTRACT.

Repetition enhancement to voice identities in the dog brain.

In the human speech signal, cues of speech sounds and voice identities are conflated, but they are processed separately in the human brain. The processing of speech sounds and voice identities is typically performed by non-primary auditory regions in humans and non-human primates. Additionally, these processes exhibit functional asymmetry in humans, indicating the involvement of distinct mechanisms. Behavioural studies indicate analogue side biases in dogs, but neural evidence for this functional dissociation is missing. In two experiments, using an fMRI adaptation paradigm, we presented awake dogs with natural human speech that either varied in segmental (change in speech sound) or suprasegmental (change in voice identity) content. In auditory regions, we found a repetition enhancement effect for voice identity processing in a secondary auditory region - the caudal ectosylvian gyrus. The same region did not show repetition effects for speech sounds, nor did the primary auditory cortex exhibit sensitivity to changes either in the segmental or in the suprasegmental content. Furthermore, we did not find evidence for functional asymmetry neither in the processing of speech sounds or voice identities. Our results in dogs corroborate former human and non-human primate evidence on the role of secondary auditory regions in the processing of suprasegmental cues, suggesting similar neural sensitivity to the identity of the vocalizer across the mammalian order.

The biological bases of colour categorisation: From goldfish to the human brain.

How are colour categories related to perception and language? To answer this question, we review research on the neural correlates of colour categories, and categorical responses in preverbal infants and non-human animals. With respect to language, the reviewed findings suggest that colour categorisation often involves automatic language processing. At the same time, evidence from non-human animals, infants, and patients with brain lesions indicates that colour categorisation may also occur in the absence of language. Concerning perception, there is little convincing evidence that the bottom-up processes of colour perception are the origin of colour categories. Instead, colour categorisation might simply build upon the continuous colour perception and interact with perception through the direction of attention to colour differences that are relevant to categorisation. We make three suggestions for future research. First, future research in all areas requires methodological improvements, in particular in stimulus control. Second, future research should overcome the universalist-realist debate and go beyond a simple contrast between perception and language. Third, the link between object colours and colour categories provides an alternative approach that might reveal the ecological origin of colour categories. The ecological approach promises establishing evolutionary and developmental continuity between categorical responses in non-human animals, infants and adult humans.

Orthographic processing deficits in developmental dyslexia: Beyond the ventral visual stream.

Fast effortless reading has been associated with the Visual Word Form Area (VWFA), a region in the ventral visual stream that specializes in the recognition of letter strings. Several neuroimaging studies of dyslexia revealed an underactivation of this region. However, most of these studies used reading tasks and/or were carried out on adults. Given that fluent reading is severely impaired in dyslexics, any underactivation might simply reflect a well-established reading deficit in impaired readers and could be the consequence rather than the cause of dyslexia. Here, we designed a task that does not rely on reading per se but that tapped early visual orthographic processing that forms the basis of reading. Dyslexic children aged 8-12years and age-matched controls were asked to search for letters, digits, and symbols in 5-element strings (Experiment 1). This novel task was complemented by a classic task known to activate the VWFA, namely the passive viewing of pseudowords and falsefonts (Experiment 2). We found that in addition to significant group differences in the VWFA, dyslexic children showed a significant underactivation of the middle occipital gyrus (MOG) relative to the control group. Several areas in the MOG are known for their engagement in visuospatial processing, and it has been proposed that the MOG is necessary for ordering the symbols in unfamiliar strings. Our results suggest that the VWFA deficit might be secondary to an impairment of visuospatial processing in the MOG. We argue that efficient processing in MOG in the course of reading acquisition is critical for the development of effortless fast visual word recognition in the VWFA.