Benjamin Wilson

Auditory sequence processing reveals evolutionarily conserved regions of frontal cortex in macaques and humans

An evolutionary account of human language as a neurobiological system must distinguish between human-unique neurocognitive processes supporting language and evolutionarily conserved, domain-general processes that can be traced back to our primate ancestors. Neuroimaging studies across species may determine whether candidate neural processes are supported by homologous, functionally conserved brain areas or by different neurobiological substrates. Here we use functional magnetic resonance imaging in Rhesus macaques and humans to examine the brain regions involved in processing the ordering relationships between auditory nonsense words in rule-based sequences. We find that key regions in the human ventral frontal and opercular cortex have functional counterparts in the monkey brain. These regions are also known to be associated with initial stages of human syntactic processing. This study raises the possibility that certain ventral frontal neural systems, which play a significant role in language function in modern humans, originally evolved to support domain-general abilities involved in sequence processing.

Implicit trustworthiness ratings of self-resembling faces activate brain centers involved in reward.

On the basis of Hamiltons (Hamilton, W. D. (1964). The genetical evolution of social behavior I, II. Journal of Theoretical Biology, 7, 17-52) theory of inclusive fitness, self-facial resemblance is hypothesized as a mechanism for self-referent phenotypic matching by which humans can detect kin. To understand the mechanisms underlying pro-sociality toward self-resembling faces, we investigated the neural correlates of implicit trustworthiness ratings for self-resembling faces. Here we show that idiosyncratic trustworthiness ratings of self-resembling faces predict brain activation in the ventral inferior, middle and medial frontal gyri, substrates involved in reward processing. These findings demonstrate that neural reward centers are implicated in evaluating implicit pro-social behaviors toward self-resembling faces. These findings suggest that humans have evolved to use neurocomputational architecture dedicated to face processing and reward evaluation for the differentiation of kin, which drives implicit idiosyncratic affectively regulated social interactions.

Conserved Sequence Processing in Primate Frontal Cortex

An important aspect of animal perception and cognition is learning to recognize relationships between environmental events that predict others in time, a form of relational knowledge that can be assessed using sequence-learning paradigms. Humans are exquisitely sensitive to sequencing relationships, and their combinatorial capacities, most saliently in the domain of language, are unparalleled. Recent comparative research in human and nonhuman primates has obtained behavioral and neuroimaging evidence for evolutionarily conserved substrates involved in sequence processing. The findings carry implications for the origins of domain-general capacities underlying core language functions in humans. Here, we synthesize this research into a ‘ventrodorsal gradient’ model, where frontal cortex engagement along this axis depends on sequencing complexity, mapping onto the sequencing capacities of different species.

Mixed‐complexity artificial grammar learning in humans and macaque monkeys: evaluating learning strategies

Artificial grammars (AG) can be used to generate rule‐based sequences of stimuli. Some of these can be used to investigate sequence‐processing computations in non‐human animals that might be related to, but not unique to, human language. Previous AG learning studies in non‐human animals have used different AGs to separately test for specific sequence‐processing abilities. However, given that natural language and certain animal communication systems (in particular, song) have multiple levels of complexity, mixed‐complexity AGs are needed to simultaneously evaluate sensitivity to the different features of the AG. Here, we tested humans and Rhesus macaques using a mixed‐complexity auditory AG, containing both adjacent (local) and non‐adjacent (longer‐distance) relationships. Following exposure to exemplary sequences generated by the AG, humans and macaques were individually tested with sequences that were either consistent with the AG or violated specific adjacent or non‐adjacent relationships. We observed a considerable level of cross‐species correspondence in the sensitivity of both humans and macaques to the adjacent AG relationships and to the statistical properties of the sequences. We found no significant sensitivity to the non‐adjacent AG relationships in the macaques. A subset of humans was sensitive to this non‐adjacent relationship, revealing interesting between‐ and within‐species differences in AG learning strategies. The results suggest that humans and macaques are largely comparably sensitive to the adjacent AG relationships and their statistical properties. However, in the presence of multiple cues to grammaticality, the non‐adjacent relationships are less salient to the macaques and many of the humans.

On the pursuit of the brain network for proto-syntactic learning in non-human primates: conceptual issues and neurobiological hypotheses

Songbirds have become impressive neurobiological models for aspects of human verbal communication because they learn to sequence their song elements, analogous, in some ways, to how humans learn to produce spoken sequences with syntactic structure. However, mammals such as non-human primates are considered to be at best limited-vocal learners and not able to sequence their vocalizations, although some of these animals can learn certain ‘artificial grammar’ sequences. Thus, conceptual issues have slowed the progress in exploring potential neurobiological homologues to language-related processes in species that are taxonomically closely related to humans. We consider some of the conceptual issues impeding a pursuit of, as we define them, ‘proto-syntactic’ capabilities and their neuronal substrates in non-human animals. We also discuss ways to better bridge comparative behavioural and neurobiological data between humans and other animals. Finally, we propose guiding neurobiological hypotheses with which we aim to facilitate the future testing of the level of correspondence between the human brain network for syntactic-learning and related neurobiological networks present in other primates. Insights from the study of non-human primates and other mammals are likely to complement those being obtained in birds to further our knowledge of the human language-related network at the cellular level.

EEG potentials associated with artificial grammar learning in the primate brain

Highlights • First combined EEG and Artificial Grammar (AG) learning study in nonhuman animals.• Early and late frontal potentials modulated in response to violations of the AG sequencing relationships in the primate brain.• Informative similarities and differences are noted in relation to reported human EEG potentials associated with AG learning.

Sequence learning modulates neural responses and oscillatory coupling in human and monkey auditory cortex

Learning complex ordering relationships between sensory events in a sequence is fundamental for animal perception and human communication. While it is known that rhythmic sensory events can entrain brain oscillations at different frequencies, how learning and prior experience with sequencing relationships affect neocortical oscillations and neuronal responses is poorly understood. We used an implicit sequence learning paradigm (an “artificial grammar”) in which humans and monkeys were exposed to sequences of nonsense words with regularities in the ordering relationships between the words. We then recorded neural responses directly from the auditory cortex in both species in response to novel legal sequences or ones violating specific ordering relationships. Neural oscillations in both monkeys and humans in response to the nonsense word sequences show strikingly similar hierarchically nested low-frequency phase and high-gamma amplitude coupling, establishing this form of oscillatory coupling—previously associated with speech processing in the human auditory cortex—as an evolutionarily conserved biological process. Moreover, learned ordering relationships modulate the observed form of neural oscillatory coupling in both species, with temporally distinct neural oscillatory effects that appear to coordinate neuronal responses in the monkeys. This study identifies the conserved auditory cortical neural signatures involved in monitoring learned sequencing operations, evident as modulations of transient coupling and neuronal responses to temporally structured sensory input.

Auditory and visual sequence learning in humans and monkeys using an artificial grammar learning paradigm

Graphical abstract

Artificial grammar learning in vascular and progressive non-fluent aphasias

ABSTRACT Patients with non‐fluent aphasias display impairments of expressive and receptive grammar. This has been attributed to deficits in processing configurational and hierarchical sequencing relationships. This hypothesis had not been formally tested. It was also controversial whether impairments are specific to language, or reflect domain general deficits in processing structured auditory sequences. Here we used an artificial grammar learning paradigm to compare the abilities of controls to participants with agrammatic aphasia of two different aetiologies: stroke and frontotemporal dementia. Ten patients with non‐fluent variant primary progressive aphasia (nfvPPA), 12 with non‐fluent aphasia due to stroke, and 11 controls implicitly learned a novel mixed‐complexity artificial grammar designed to assess processing of increasingly complex sequencing relationships. We compared response profiles for otherwise identical sequences of speech tokens (nonsense words) and tone sweeps. In all three groups the ability to detect grammatical violations varied with sequence complexity, with performance improving over time and being better for adjacent than non‐adjacent relationships. Patients performed less well than controls overall, and this was related more strongly to aphasia severity than to aetiology. All groups improved with practice and performed well at a control task of detecting oddball nonwords. Crucially, group differences did not interact with sequence complexity, demonstrating that aphasic patients were not disproportionately impaired on complex structures. Hierarchical cluster analysis revealed that response patterns were very similar across all three groups, but very different between the nonsense word and tone tasks, despite identical artificial grammar structures. Overall, we demonstrate that agrammatic aphasics of two different aetiologies are not disproportionately impaired on complex sequencing relationships, and that the learning of phonological and non‐linguistic sequences occurs independently. The similarity of profiles of discriminatory abilities and rule learning across groups suggests that insights from previous studies of implicit sequence learning in vascular aphasia are likely to prove applicable in nfvPPA. HIGHLIGHTSPatients with Brocas aphasia and nfvPPA show implicit artificial grammar learning.Both groups displayed global deficits compared to controls but improved with practice.Neither group was disproportionately impaired on more complex ordering relationships.Learning did not transfer between otherwise identical speech and tone‐based grammars.Separate linguistic and non‐linguistic sequence processing was maintained in aphasia.

Individually customisable non-invasive head immobilisation system for non-human primates with an option for voluntary engagement

Highlights • Non-invasive head immobilisation for neuroscience experiments in monkeys.• Individually customised system combining functionality of previous systems.• Allows access for auditory and visual stimulation.• Has the option for voluntary engagement to assist habituation.• Systematically evaluated against scientific and animal welfare needs.