From active affordance to active inference: vertical integration of cognition in the cerebral cortex through dual subcortical control systems.

In previous papers, we proposed that the dorsal attention system's top-down control is regulated by the dorsal division of the limbic system, providing a feedforward or impulsive form of control generating expectancies during active inference. In contrast, we proposed that the ventral attention system is regulated by the ventral limbic division, regulating feedback constraints and error-correction for active inference within the neocortical hierarchy. Here, we propose that these forms of cognitive control reflect vertical integration of subcortical arousal control systems that evolved for specific forms of behavior control. The feedforward impetus to action is regulated by phasic arousal, mediated by lemnothalamic projections from the reticular activating system of the lower brainstem, and then elaborated by the hippocampus and dorsal limbic division. In contrast, feedback constraint-based on environmental requirements-is regulated by the tonic activation furnished by collothalamic projections from the midbrain arousal control centers, and then sustained and elaborated by the amygdala, basal ganglia, and ventral limbic division. In an evolutionary-developmental analysis, understanding these differing forms of active affordance-for arousal and motor control within the subcortical vertebrate neuraxis-may help explain the evolution of active inference regulating the cognition of expectancy and error-correction within the mammalian 6-layered neocortex.

Adaptive control of functional connectivity: dorsal and ventral limbic divisions regulate the dorsal and ventral neocortical networks.

The connectional anatomy of the primate cortex is now well-defined by the Structural Model, in which adjacent cortical areas are interconnected in an organized network hierarchy of communication and control. The computational theory of "active inference" can be aligned with this architecture, proposing that predictions descend from higher association areas to be updated by ascending prediction errors from lower (i.e. primary) sensory and motor areas. Given the connectivity, the limbic networks at the apex of the cerebral hierarchy must then be responsible for the most general expectancies, which are propagated through the hierarchy to organize the multiple component network levels of experience and behavior. Anatomical evidence suggests that there are dual limbic divisions, reflecting archicortical (dorsal) and paleocortical (ventral) derivations, resulting in fundamentally different neural mechanisms for managing expectancies across the corticolimbic hierarchy. In the functional connectivity literature, the dorsal attention network is seen to provide top-down or endogenous control of attention, whereas the ventral attention network provides stimulus bound or exogenous attentional control. We review evidence indicating that the dorsal, archicortical division of the limbic system provides a feedforward, impulsive, endogenous mode of motive control, whereas the ventral, paleocortical limbic division provides feedback constraint linked to exogenous events.

Feasibility of a Personal Neuromorphic Emulation.

The representation of intelligence is achieved by patterns of connections among neurons in brains and machines. Brains grow continuously, such that their patterns of connections develop through activity-dependent specification, with the continuing ontogenesis of individual experience. The theory of active inference proposes that the developmental organization of sentient systems reflects general processes of informatic self-evidencing, through the minimization of free energy. We interpret this theory to imply that the mind may be described in information terms that are not dependent on a specific physical substrate. At a certain level of complexity, self-evidencing of living (self-organizing) information systems becomes hierarchical and reentrant, such that effective consciousness emerges as the consequence of a good regulator. We propose that these principles imply that an adequate reconstruction of the computational dynamics of an individual human brain/mind is possible with sufficient neuromorphic computational emulation.

Continuity and change in neural plasticity through embryonic morphogenesis, fetal activity-dependent synaptogenesis, and infant memory consolidation.

There is an apparent continuity in human neural development that can be traced to venerable themes of vertebrate morphogenesis that have shaped the evolution of the reptilian telencephalon (including both primitive three-layered cortex and basal ganglia) and then the subsequent evolution of the mammalian six-layered neocortex. In this theoretical analysis, we propose that an evolutionary-developmental analysis of these general morphogenetic themes can help to explain the embryonic development of the dual divisions of the limbic system that control the dorsal and ventral networks of the human neocortex. These include the archicortical (dorsal limbic) Papez circuits regulated by the hippocampus that organize spatial, contextual memory, as well as the paleocortical (ventral limbic) circuits that organize object memory. We review evidence that these dorsal and ventral limbic divisions are controlled by the differential actions of brainstem lemnothalamic and midbrain collothalamic arousal control systems, respectively, thereby traversing the vertebrate subcortical neuraxis. These dual control systems are first seen shaping the phyletic morphogenesis of the archicortical and paleocortical foundations of the forebrain in embryogenesis. They then provide dual modes of activity-dependent synaptic organization in the active (lemnothalamic) and quiet (collothalamic) stages of fetal sleep. Finally, these regulatory systems mature to form the major systems of memory consolidation of postnatal development, including the rapid eye movement (lemnothalamic) consolidation of implicit memory and social attachment in the first year, and then-in a subsequent stage-the non-REM (collothalamic) consolidation of explicit memory that is integral to the autonomy and individuation of the second year of life.

Neurophysiological mechanisms of implicit and explicit memory in the process of consciousness.

Neurophysiological mechanisms are increasingly understood to constitute the foundations of human conscious experience. These include the capacity for ongoing memory, achieved through a hierarchy of reentrant cross-laminar connections across limbic, heteromodal, unimodal, and primary cortices. The neurophysiological mechanisms of consciousness also include the capacity for volitional direction of attention to the ongoing cognitive process, through a reentrant fronto-thalamo-cortical network regulation of the inhibitory thalamic reticular nucleus. More elusive is the way that discrete objects of subjective experience, such as the color of deep blue or the sound of middle C, could be generated by neural mechanisms. Explaining such ineffable qualities of subjective experience is what Chalmers has called "the hard problem of consciousness," which has divided modern neuroscientists and philosophers alike. We propose that insight into the appearance of the hard problem can be gained through integrating classical phenomenological studies of experience with recent progress in the differential neurophysiology of consolidating explicit versus implicit memory. Although the achievement of consciousness, once it is reflected upon, becomes explicit, the underlying process of generating consciousness, through neurophysiological mechanisms, is largely implicit. Studying the neurophysiological mechanisms of adaptive implicit memory, including brain stem, limbic, and thalamic regulation of neocortical representations, may lead to a more extended phenomenological understanding of both the neurophysiological process and the subjective experience of consciousness.NEW & NOTEWORTHY The process of consciousness, generating the qualia that may appear to be irreducible qualities of experience, can be understood to arise from neurophysiological mechanisms of memory. Implicit memory, organized by the lemnothalamic brain stem projections and dorsal limbic consolidation in REM sleep, supports the unconscious field and the quasi-conscious fringe of current awareness. Explicit memory, organized by the collothalamic midbrain projections and ventral limbic consolidation of NREM sleep, supports the focal objects of consciousness.

Critical periods for the neurodevelopmental processes of externalizing and internalizing.

Research on neurobiological development is providing insight into the nature and mechanisms of human neural plasticity. These mechanisms appear to support two different forms of developmental learning. One form of learning could be described as externalizing, in which neural representations are highly responsive to environmental influences, as the child typically operates under a mode of hedonic approach. A second form of learning supports internalizing, in which motive control separates attention and self-regulation from the immediate influences of the context, particularly when the child faces conditions of avoidance and threat. The dorsal cortical networks of externalizing are organized around dorsal limbic (cingulate, septal, lateral hypothalamic, hippocampal, and ventral striatal) circuits. In contrast, the ventral cortical networks of internalizing are organized around ventral limbic (anterior temporal and orbital cortex, extended amygdala, dorsal striatal, and mediodorsal thalamic) circuits. These dual divisions of the limbic system in turn self-regulate their arousal levels through different brain stem and forebrain neuromodulator projection systems, with dorsal corticolimbic networks regulated strongly by locus coeruleus norepinephrine and brain stem raphe nucleus serotonin projection systems, and ventral corticolimbic networks regulated by ventral tegmental dopamine and forebrain acetylcholine projections. Because the arousal control systems appear to regulate specific properties of neural plasticity in development, an analysis of these systems explains differences between externalizing and internalizing at multiple levels of neural and psychological self-regulation. In neuroscience, the concept of critical periods has been applied to times when experience is essential for the maturation of sensory systems. In a more general neuropsychological analysis, certain periods of the child's development require successful self-regulation through the differential capacities for externalizing and internalizing.

Computational modeling of human head electromagnetics for source localization of milliscale brain dynamics.

Understanding the milliscale (temporal and spatial) dynamics of the human brain activity requires high-resolution modeling of head electromagnetics and source localization of EEG data. We have developed an automated environment to construct individualized computational head models from image segmentation and to estimate conductivity parameters using electrical impedance tomography methods. Algorithms incorporating tissue inhomogeneity and impedance anisotropy in electromagnetics forward simulations have been developed and parallelized. The paper reports on the application of the environment in the processing of realistic head models, including conductivity inverse estimation and lead field generation for use in EEG source analysis.

Motive control of unconscious inference: The limbic base of adaptive Bayes.

Current computational models of neocortical processing, described as predictive coding theory, are providing new ways of understanding Helmholtz's classical insight that perception cannot proceed in a data-driven fashion, but instead requires unconscious inference based on prior experience. Predictive coding is a Bayesian process, in which the operations at each lower level of the cortical hierarchy are predicted by prior projections of expectancies from a higher level, and are then updated by error-correction with lower level evidence. To generalize the predictive coding model to the human neocortex as a whole requires aligning the Bayesian negotiation of prior expectancies with sensory and motor evidence not only within the connectional architecture of the neocortex (primary sensory/motor, unimodal association areas, and heteromodal association areas) but also with the limbic cortex that forms the base for the adaptive control of the heteromodal areas and thereby the cerebral hemisphere as a whole. By reviewing the current evidence on the anatomy of the human corticolimbic connectivity (now formalized as the Structural Model) we address the problem of how limbic cortex resonates to the homeostatic, personal significance of events to provide Bayesian priors to organize the operations of predictive coding across the multiple levels of the neocortex. By reviewing both classical evidence and current models of control exerted between limbic and neocortical networks, we suggest a neuropsychological theory of human cognition, the adaptive Bayes process model, in which prior expectancies are not simply rationalized propositions, but rather affectively-charged expectancies that bias the interpretation of sensory data and action affordances to support allostasis, the motive control of expectancies for future events.

Source localization of epileptic spikes using Multiple Sparse Priors.

OBJECTIVE: To evaluate epileptic source estimation using multiple sparse priors (MSP) inverse method and high-resolution, individual electrical head models. METHODS: Accurate source localization is dependent on accurate electrical head models and appropriate inverse solvers. Using high-resolution, individual electrical head models in fifteen epilepsy patients, with surgical resection and clinical outcome as criteria for accuracy, performance of MSP method was compared against standardized low-resolution brain electromagnetic tomography (sLORETA) and coherent maximum entropy on the mean (cMEM) methods. RESULTS: The MSP method performed similarly to the sLORETA method and slightly better than the cMEM method in terms of success rate. The MSP and cMEM methods were more focal than sLORETA with the advantage of not requiring an arbitrary selection of a hyperparameter or thresholding of reconstructed current density values to determine focus. MSP and cMEM methods were better than sLORETA in terms of spatial dispersion. CONCLUSIONS: Results suggest that the three methods are complementary and could be used together. In practice, the MSP method will be easier to use and interpret compared to sLORETA, and slightly more accurate and faster than the cMEM method. SIGNIFICANCE: Source localization of interictal spikes from dense-array electroencephalography data has been shown to be a reliable marker of epileptic foci and useful for pre-surgical planning. The advantages of MSP make it a useful complement to other inverse solvers in clinical practice.

Transcranial Electrical Stimulation targeting limbic cortex increases the duration of human deep sleep.

BACKGROUND: Researchers have proposed that impaired sleep may be a causal link in the progression from Mild Cognitive Impairment (MCI) to Alzheimer's Disease (AD). Several recent findings suggest that enhancing deep sleep (N3) may improve neurological health in persons with MCI, and buffer the risk for AD. Specifically, Transcranial Electrical Stimulation (TES) of frontal brain areas, the inferred source of the Slow Oscillations (SOs) of N3 sleep, can extend N3 sleep duration and improve declarative memory for recently learned information. Recent work in our laboratory using dense array Electroencephalography (dEEG) localized the sources of SOs to anterior limbic sites - suggesting that targeting these sites with TES may be more effective for enhancing N3. METHODS: For the present study, we recruited 13 healthy adults (M = 42 years) to participate in three all-night sleep EEG recordings where they received low level (0.5 mA) TES designed to target anterior limbic areas and a sham stimulation (placebo). We used a convolutional neural network, trained and tested on professionally scored EEG sleep staging, to predict sleep stages for each recording. RESULTS: When compared to the sham session, limbic-targeted TES significantly increased the duration of N3 sleep. TES also significantly increased spectral power in the 0.5-1 Hz frequency band (relative to pre-TES epochs) in left temporoparietal and left occipital scalp regions compared to sham. CONCLUSION: These results suggest that even low-level TES, when specifically targeting anterior limbic sites, can increase deep (N3) sleep and thereby contribute to healthy sleep quality.