Recruitment and Consolidation of Cell Assemblies for Words by Way of Hebbian Learning and Competition in a Multi-Layer Neural Network

Current cognitive theories postulate either localist representations of knowledge or fully overlapping, distributed ones. We use a connectionist model that closely replicates known anatomical properties of the cerebral cortex and neurophysiological principles to show that Hebbian learning in a multi-layer neural network leads to memory traces (cell assemblies) that are both distributed and anatomically distinct. Taking the example of word learning based on action-perception correlation, we document mechanisms underlying the emergence of these assemblies, especially (i) the recruitment of neurons and consolidation of connections defining the kernel of the assembly along with (ii) the pruning of the cell assembly’s halo (consisting of very weakly connected cells). We found that, whereas a learning rule mapping covariance led to significant overlap and merging of assemblies, a neurobiologically grounded synaptic plasticity rule with fixed LTP/LTD thresholds produced minimal overlap and prevented merging, exhibiting competitive learning behaviour. Our results are discussed in light of current theories of language and memory. As simulations with neurobiologically realistic neural networks demonstrate here spontaneous emergence of lexical representations that are both cortically dispersed and anatomically distinct, both localist and distributed cognitive accounts receive partial support

Neurobiological mechanisms for language, symbols and concepts: Clues from brain-constrained deep neural networks

Neural networks are successfully used to imitate and model cognitive processes. However, to provide clues about the neurobiological mechanisms enabling human cognition, these models need to mimic the structure and function of real brains. Brain-constrained networks differ from classic neural networks by implementing brain similarities at different scales, ranging from the micro- and mesoscopic levels of neuronal function, local neuronal links and circuit interaction to large-scale anatomical structure and between-area connectivity. This review shows how brain-constrained neural networks can be applied to study in silico the formation of mechanisms for symbol and concept processing and to work towards neurobiological explanations of specifically human cognitive abilities. These include verbal working memory and learning of large vocabularies of symbols, semantic binding carried by specific areas of cortex, attention focusing and modulation driven by symbol type, and the acquisition of concrete and abstract concepts partly influenced by symbols. Neuronal assembly activity in the networks is analyzed to deliver putative mechanistic correlates of higher cognitive processes and to develop candidate explanations founded in established neurobiological principles

The Role of Synaptic Tagging and Capture for Memory Dynamics in Spiking Neural Networks

Memory serves to process and store information about experiences such that this information can be used in future situations. The transfer from transient storage into long-term memory, which retains information for hours, days, and even years, is called consolidation. In brains, information is primarily stored via alteration of synapses, so-called synaptic plasticity. While these changes are at first in a transient early phase, they can be transferred to a late phase, meaning that they become stabilized over the course of several hours. This stabilization has been explained by so-called synaptic tagging and capture (STC) mechanisms. To store and recall memory representations, emergent dynamics arise from the synaptic structure of recurrent networks of neurons. This happens through so-called cell assemblies, which feature particularly strong synapses. It has been proposed that the stabilization of such cell assemblies by STC corresponds to so-called synaptic consolidation, which is observed in humans and other animals in the first hours after acquiring a new memory. The exact connection between the physiological mechanisms of STC and memory consolidation remains, however, unclear. It is equally unknown which influence STC mechanisms exert on further cognitive functions that guide behavior. On timescales of minutes to hours (that means, the timescales of STC) such functions include memory improvement, modification of memories, interference and enhancement of similar memories, and transient priming of certain memories. Thus, diverse memory dynamics may be linked to STC, which can be investigated by employing theoretical methods based on experimental data from the neuronal and the behavioral level. In this thesis, we present a theoretical model of STC-based memory consolidation in recurrent networks of spiking neurons, which are particularly suited to reproduce biologically realistic dynamics. Furthermore, we combine the STC mechanisms with calcium dynamics, which have been found to guide the major processes of early-phase synaptic plasticity in vivo. In three included research articles as well as additional sections, we develop this model and investigate how it can account for a variety of behavioral effects. We find that the model enables the robust implementation of the cognitive memory functions mentioned above. The main steps to this are: 1. demonstrating the formation, consolidation, and improvement of memories represented by cell assemblies, 2. showing that neuromodulator-dependent STC can retroactively control whether information is stored in a temporal or rate-based neural code, and 3. examining interaction of multiple cell assemblies with transient and attractor dynamics in different organizational paradigms. In summary, we demonstrate several ways by which STC controls the late-phase synaptic structure of cell assemblies. Linking these structures to functional dynamics, we show that our STC-based model implements functionality that can be related to long-term memory. Thereby, we provide a basis for the mechanistic explanation of various neuropsychological effects.2021-09-0

Formation of neocortical memory circuits for unattended written word forms : neuromagnetic evidence

To master linguistic communication, humans must acquire large vocabularies quickly and effortlessly. Efficient word learning might be facilitated by the ability to rapidly acquire novel word forms even outside the focus of attention, occurring within minutes of repetitive exposure and suggesting fast and automatic lexicon acquisition. However, this phenomenon has been studied in the auditory modality only, and it is unknown whether similar mechanisms also exist in the visual domain. We tested this by presenting participants with novel written word forms while the focus of their attention was on a non-linguistic dual colour-detection task. Matched familiar word forms served as a control. Using magnetoencephalography (MEG), we scrutinised changes in neuromagnetic responses to familiar and to novel word forms over approximately 15 minutes of exposure. We found, for the first time, a visual analogue of automatic rapid build-up of neural memory circuits for unattended novel lexical items, seen as a rapid enhancement of early (similar to 100 ms post-onset) activation in the left anterior-superior temporal lobe. Our results suggest that the brain quickly forms cortical representations for new written forms, and indicate that the automatic neural mechanisms subserving rapid online acquisition of novel linguistic information might be shared by both auditory and visual modalities.Peer reviewe

Adaptive learning in a compartmental model of visual cortex—how feedback enables stable category learning and refinement

The categorization of real world objects is often reflected in the similarity of their visual appearances. Such categories of objects do not necessarily form disjunct sets of objects, neither semantically nor visually. The relationship between categories can often be described in terms of a hierarchical structure. For instance, tigers and leopards build two separate mammalian categories, but both belong to the category of felines. In other words, tigers and leopards are subcategories of the category Felidae. In the last decades, the unsupervised learning of categories of visual input stimuli has been addressed by numerous approaches in machine learning as well as in the computational neurosciences. However, the question of what kind of mechanisms might be involved in the process of subcategory learning, or category refinement, remains a topic of active investigation. We propose a recurrent computational network architecture for the unsupervised learning of categorial and subcategorial visual input representations. During learning, the connection strengths of bottom-up weights from input to higher-level category representations are adapted according to the input activity distribution. In a similar manner, top-down weights learn to encode the characteristics of a specific stimulus category. Feedforward and feedback learning in combination realize an associative memory mechanism, enabling the selective top-down propagation of a category's feedback weight distribution. We suggest that the difference between the expected input encoded in the projective field of a category node and the current input pattern controls the amplification of feedforward-driven representations. Large enough differences trigger the recruitment of new representational resources and the establishment of (sub-) category representations. We demonstrate the temporal evolution of such learning and show how the approach successully establishes category and subcategory representations

Visual cortex recruitment during language processing in blind individuals is explained by Hebbian learning

In blind people, the visual cortex takes on higher cognitive functions, including language. Why this functional organisation mechanistically emerges at the neuronal circuit level is still unclear. Here, we use a biologically constrained network model implementing features of anatomical structure, neurophysiological function and connectivity of fronto-temporal-occipital areas to simulate word-meaning acquisition in visually deprived and undeprived brains. We observed that, only under visual deprivation, distributed word-related neural circuits ‘grew into’ the deprived visual areas, which therefore adopted a linguistic-semantic role. Three factors are crucial for explaining this deprivation-related growth: changes in the network’s activity balance brought about by the absence of uncorrelated sensory input, the connectivity structure of the network, and Hebbian correlation learning. In addition, the blind model revealed long-lasting spiking neural activity compared to the sighted model during word recognition, which is a neural correlate of enhanced verbal working memory. The present neurocomputational model offers a neurobiological account for neural changes followed by sensory deprivation, thus closing the gap between cellular-level mechanisms, system-level linguistic and semantic function

Learning Visual-Motor Cell Assemblies for the iCub Robot using a Neuroanatomically Grounded Neural Network

In this work we describe how an existing neural model for learning Cell Assemblies (CAs) across multiple neuroanatomical brain areas has been integrated with a humanoid robot simulation to explore the learning of associations of visual and motor modalities. The results show that robust CAs are learned to enable pattern completion to select a correct motor response when only visual input is presented. We also show, with some parameter tuning and the pre-processing of more realistic patterns taken from images of real objects and robot poses the network can act as a controller for the robot in visuo-motor association tasks. This provides the basis for further neurorobotic experiments on grounded language learning

Breakdown of category-specific word representations in a brain-constrained neurocomputational model of semantic dementia

The neurobiological nature of semantic knowledge, i.e., the encoding and storage of conceptual information in the human brain, remains a poorly understood and hotly debated subject. Clinical data on semantic deficits and neuroimaging evidence from healthy individuals have suggested multiple cortical regions to be involved in the processing of meaning. These include semantic hubs (most notably, anterior temporal lobe, ATL) that take part in semantic processing in general as well as sensorimotor areas that process specific aspects/categories according to their modality. Biologically inspired neurocomputational models can help elucidate the exact roles of these regions in the functioning of the semantic system and, importantly, in its breakdown in neurological deficits. We used a neuroanatomically constrained computational model of frontotemporal cortices implicated in word acquisition and processing, and adapted it to simulate and explain the effects of semantic dementia (SD) on word processing abilities. SD is a devastating, yet insufficiently understood progressive neurodegenerative disease, characterised by semantic knowledge deterioration that is hypothesised to be specifically related to neural damage in the ATL. The behaviour of our brain-based model is in full accordance with clinical data—namely, word comprehension performance decreases as SD lesions in ATL progress, whereas word repetition abilities remain less affected. Furthermore, our model makes predictions about lesion- and category-specific effects of SD: our simulation results indicate that word processing should be more impaired for object- than for action-related words, and that degradation of white matter should produce more severe consequences than the same proportion of grey matter decay. In sum, the present results provide a neuromechanistic explanatory account of cortical-level language impairments observed during the onset and progress of semantic dementia

Geometry and Topology in Memory and Navigation

Okinawa Institute of Science and Technology Graduate UniversityDoctor of PhilosophyGeometry and topology offer rich mathematical worlds and perspectives with which to study and improve our understanding of cognitive function. Here I present the following examples: (1) a functional role for inhibitory diversity in associative memories with graph- ical relationships; (2) improved memory capacity in an associative memory model with setwise connectivity, with implications for glial and dendritic function; (3) safe and effi- cient group navigation among conspecifics using purely local geometric information; and　(4) enhancing geometric and topological methods to probe the relations between neural activity and behaviour. In each work, tools and insights from geometry and topology are used in essential ways to gain improved insights or performance. This thesis contributes to our knowledge of the potential computational affordances of biological mechanisms (such as inhibition and setwise connectivity), while also demonstrating new geometric and topological methods and perspectives with which to deepen our understanding of cognitive tasks and their neural representations.doctoral thesi

The role of excitation and inhibition in learning and memory formation

The neurons in the mammalian brain can be classified into two broad categories: excitatory and inhibitory neurons. The former has been historically associated to information processing whereas the latter has been linked to network homeostasis. More recently, inhibitory neurons have been related to several computational roles such as the gating of signal propagation, mediation of network competition, or learning. However, the ways by which excitation and inhibition can regulate learning have not been exhaustively explored. Here we explore several model systems to investigate the role of excitation and inhibition in learning and memory formation. Additionally, we investigate the effect that third factors such as neuromodulators and network state exert over this process. Firstly, we explore the effect of neuromodulators onto excitatory neurons and excitatory plasticity. Next, we investigate the plasticity rules governing excitatory connections while the neural network oscillates in a sleep-like cycle, shifting between Up and Down states. We observe that this plasticity rule depends on the state of the network. To study the role of inhibitory neurons in learning, we then investigate the mechanisms underlying place field emergence and consolidation. Our simulations suggest that dendrite-targeting interneurons play an important role in both promoting the emergence of new place fields and in ensuring place field stabilization. Soma-targeting interneurons, on the other hand, are suggested to be related to quick, context-specific changes in the assignment of place and silent cells. We next investigate the mechanisms underlying the plasticity of synaptic connections from specific types of interneurons. Our experiments suggest that different types of interneurons undergo different synaptic plasticity rules. Using a computational model, we implement these plasticity rules in a simplified network. Our simulations indicate that the interaction between the different forms of plasticity account for the development of stable place fields across multiple environments. Moreover, these plasticity rules seems to be gated by the postsynaptic membrane voltage. Inspired by these findings, we propose a voltage-based inhibitory synaptic plasticity rule. As a consequence of this rule, the network activity is kept controlled by the imposition of a maximum pyramidal cell firing rate. Remarkably, this rule does not constrain the postsynaptic firing rate to a narrow range. Overall, through multiple stages of interactions between experiments and computational simulations, we investigate the effect of excitation and inhibition in learning. We propose mechanistic explanations for experimental data, and suggest possible functional implications of experimental findings. Finally, we proposed a voltage-based inhibitory synaptic plasticity model as a mechanism for flexible network homeostasis.Open Acces