Interactive neurorobotics: Behavioral and neural dynamics of agent interactions.

Interactive neurorobotics is a subfield which characterizes brain responses evoked during interaction with a robot, and their relationship with the behavioral responses. Gathering rich neural and behavioral data from humans or animals responding to agents can act as a scaffold for the design process of future social robots. This research seeks to study how organisms respond to artificial agents in contrast to biological or inanimate ones. This experiment uses the novel affordances of the robotic platforms to investigate complex dynamics during minimally structured interactions that would be difficult to capture with classical experimental setups. We then propose a general framework for such experiments that emphasizes naturalistic interactions combined with multimodal observations and complementary analysis pipelines that are necessary to render a holistic picture of the data for the purpose of informing robotic design principles. Finally, we demonstrate this approach with an exemplar rat-robot social interaction task which included simultaneous multi-agent tracking and neural recordings.

Convergent cross sorting for estimating dynamic coupling.

Natural systems exhibit diverse behavior generated by complex interactions between their constituent parts. To characterize these interactions, we introduce Convergent Cross Sorting (CCS), a novel algorithm based on convergent cross mapping (CCM) for estimating dynamic coupling from time series data. CCS extends CCM by using the relative ranking of distances within state-space reconstructions to improve the prior methods' performance at identifying the existence, relative strength, and directionality of coupling across a wide range of signal and noise characteristics. In particular, relative to CCM, CCS has a large performance advantage when analyzing very short time series data and data from continuous dynamical systems with synchronous behavior. This advantage allows CCS to better uncover the temporal and directional relationships within systems that undergo frequent and short-lived switches in dynamics, such as neural systems. In this paper, we validate CCS on simulated data and demonstrate its applicability to electrophysiological recordings from interacting brain regions.

Spatial learning in male and female Long-Evans rats.

Male and female Long-Evans rats were tested in the Morris water maze at 6 months of age. A place training procedure, in which rats learned the position of a camouflaged platform, was followed by cue training, in which rats escaped to a visible platform. No sex difference was found in place learning ability. Search accuracy on probe trials, when the platform was unavailable, was also equivalent for the male and female groups. These results contrast with previous studies of rodents at younger ages, which have reported a male advantage in spatial learning. It is suggested that the age at which rats are assessed may be an important factor, possibly reflecting a different course in the relatively protracted maturation of the hippocampus in male and female rats. The results of this investigation are also discussed with reference to studies of sex differences for spatial abilities in humans. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Can a robot teach me that? Children's ability to imitate robots.

Commensurate with constant technological advances, social robots are increasingly anticipated to enter homes and classrooms; however, little is known about the efficacy of social robots as teaching tools. To investigate children's learning from robots, 1- to 3-year-olds observed either a human or a robot demonstrate two goal-directed object manipulation tasks and were then given the opportunity to act on the objects. Children exhibited less imitation from robotic models that varied with task complexity and age, a phenomenon we term the "robot deficit." In addition, the more children engaged with the robot prior to administration of the imitation task, the more likely they were to replicate the robot's actions. These findings document how children are able to learn from robots but that ongoing design of robotic platforms needs to be oriented to developing more socially engaging means of interacting.

One Tap at a Time: Correlating Sensorimotor Synchronization with Brain Signatures of Temporal Processing.

The ability to integrate our perceptions across sensory modalities and across time, to execute and coordinate movements, and to adapt to a changing environment rests on temporal processing. Timing is essential for basic daily tasks, such as walking, social interaction, speech and language comprehension, and attention. Impaired temporal processing may contribute to various disorders, from attention-deficit hyperactivity disorder and schizophrenia to Parkinson's disease and dementia. The foundational importance of timing ability has yet to be fully understood; and popular tasks used to investigate behavioral timing ability, such as sensorimotor synchronization (SMS), engage a variety of processes in addition to the neural processing of time. The present study utilizes SMS in conjunction with a separate passive listening task that manipulates temporal expectancy while recording electroencephalographic data. Participants display a larger N1-P2 evoked potential complex to unexpected beats relative to temporally predictable beats, a differential we call the timing response index (TRI). The TRI correlates with performance on the SMS task: better synchronizers show a larger brain response to unexpected beats. The TRI, derived from the perceptually driven N1-P2 complex, disentangles the perceptual and motor components inherent in SMS and thus may serve as a neural marker of a more general temporal processing.

Neurobiologically Inspired Self-Monitoring Systems.

In this article, we explore neurobiological principles that could be deployed in systems requiring self-preservation, adaptive control, and contextual awareness. We start with low-level control for sensor processing and motor reflexes. We then discuss how critical it is at an intermediate level to maintain homeostasis and predict system set points. We end with a discussion at a high-level, or cognitive level, where planning and prediction can further monitor the system and optimize performance. We emphasize the information flow between these levels both from a systems neuroscience and an engineering point of view. Throughout the paper, we describe the brain systems that carry out these functions and provide examples from artificial intelligence, machine learning, and robotics that include these features. Our goal is to show how biological organisms performing self-monitoring can inspire the design of autonomous and embedded systems.

Specific Basal Forebrain-Cortical Cholinergic Circuits Coordinate Cognitive Operations.

Based on recent molecular genetics, as well as functional and quantitative anatomical studies, the basal forebrain (BF) cholinergic projections, once viewed as a diffuse system, are emerging as being remarkably specific in connectivity. Acetylcholine (ACh) can rapidly and selectively modulate activity of specific circuits and ACh release can be coordinated in multiple areas that are related to particular aspects of cognitive processing. This review discusses how a combination of multiple new approaches with more established techniques are being used to finally reveal how cholinergic neurons, together with other BF neurons, provide temporal structure for behavior, contribute to local cortical state regulation, and coordinate activity between different functionally related cortical circuits. ACh selectively modulates dynamics for encoding and attention within individual cortical circuits, allows for important transitions during sleep, and shapes the fidelity of sensory processing by changing the correlation structure of neural firing. The importance of this system for integrated and fluid behavioral function is underscored by its disease-modifying role; the demise of BF cholinergic neurons has long been established in Alzheimer's disease and recent studies have revealed the involvement of the cholinergic system in modulation of anxiety-related circuits. Therefore, the BF cholinergic system plays a pivotal role in modulating the dynamics of the brain during sleep and behavior, as foretold by the intricacies of its anatomical map.

Multiplexed oscillations and phase rate coding in the basal forebrain.

Complex behaviors demand temporal coordination among functionally distinct brain regions. The basal forebrain's afferent and efferent structure suggests a capacity for mediating this coordination at a large scale. During performance of a spatial orientation task, synaptic activity in this region was dominated by four amplitude-independent oscillations temporally organized by the phase of the slowest, a theta-frequency rhythm. Oscillation amplitudes were also organized by task epoch and positively correlated to the task-related modulation of individual neuron firing rates. For many neurons, spiking was temporally organized through phase precession against theta band field potential oscillations. Theta phase precession advanced in parallel to task progression, rather than absolute spatial location or time. Together, the findings reveal a process by which associative brain regions can integrate independent oscillatory inputs and transform them into sequence-specific, rate-coded outputs that are adaptive to the pace with which organisms interact with their environment.

Cholinergic shaping of neural correlations.

A primary function of the brain is to form representations of the sensory world. Its capacity to do so depends on the relationship between signal correlations, associated with neuronal receptive fields, and noise correlations, associated with neuronal response variability. It was recently shown that the behavioral relevance of sensory stimuli can modify the relationship between signal and noise correlations, presumably increasing the encoding capacity of the brain. In this work, we use data from the visual cortex of the awake mouse watching naturalistic stimuli and show that a similar modification is observed under heightened cholinergic modulation. Increasing cholinergic levels in the cortex through optogenetic stimulation of basal forebrain cholinergic neurons decreases the dependency that is commonly observed between signal and noise correlations. Simulations of correlated neural networks with realistic firing statistics indicate that this change in the correlation structure increases the encoding capacity of the network.

Theta and beta oscillatory dynamics in the dentate gyrus reveal a shift in network processing state during cue encounters.

The hippocampus is an important structure for learning and memory processes, and has strong rhythmic activity. Although a large amount of research has been dedicated toward understanding the rhythmic activity in the hippocampus during exploratory behaviors, specifically in the theta (5-10 Hz) frequency range, few studies have examined the temporal interplay of theta and other frequencies during the presentation of meaningful cues. We obtained in vivo electrophysiological recordings of local field potentials (LFP) in the dentate gyrus (DG) of the hippocampus as rats performed three different associative learning tasks. In each task, cue presentations elicited pronounced decrements in theta amplitude in conjunction with increases in beta (15-30 Hz) amplitude. These changes were often transient but were sustained from the onset of cue encounters until the occurrence of a reward outcome. This oscillatory profile shifted in time to precede cue encounters over the course of the session, and was not present during similar behaviors in the absence of task relevant stimuli. The observed decreases in theta amplitude and increases in beta amplitude in the DG may thus reflect a shift in processing state that occurs when encountering meaningful cues.

Cell assemblies of the basal forebrain.

The basal forebrain comprises several heterogeneous neuronal subgroupings having modular projection patterns to discrete sets of cortical subregions. Each cortical region forms recurrent projections, via prefrontal cortex, that reach the specific basal forebrain subgroups from which they receive afferents. This architecture enables the basal forebrain to selectively modulate cortical responsiveness according to current processing demands. Theoretically, optimal functioning of this distributed network would be enhanced by temporal coordination among coactive basal forebrain neurons, or the emergence of "cell assemblies." The present work demonstrates assembly formation in rat basal forebrain neuronal populations during a selective attention task. Neuron pairs exhibited coactivation patterns organized within beta-frequency time windows (55 ms), regardless of their membership within distinct bursting versus nonbursting basal forebrain subpopulations. Thus, the results reveal a specific temporal framework for integration of information within basal forebrain networks and for the modulation of cortical responsiveness.

Task-phase-specific dynamics of basal forebrain neuronal ensembles.

Cortically projecting basal forebrain neurons play a critical role in learning and attention, and their degeneration accompanies age-related impairments in cognition. Despite the impressive anatomical and cell-type complexity of this system, currently available data suggest that basal forebrain neurons lack complexity in their response fields, with activity primarily reflecting only macro-level brain states such as sleep and wake, onset of relevant stimuli and/or reward obtainment. The current study examined the spiking activity of basal forebrain neuron populations across multiple phases of a selective attention task, addressing, in particular, the issue of complexity in ensemble firing patterns across time. Clustering techniques applied to the full population revealed a large number of distinct categories of task-phase-specific activity patterns. Unique population firing-rate vectors defined each task phase and most categories of task-phase-specific firing had counterparts with opposing firing patterns. An analogous set of task-phase-specific firing patterns was also observed in a population of posterior parietal cortex neurons. Thus, consistent with the known anatomical complexity, basal forebrain population dynamics are capable of differentially modulating their cortical targets according to the unique sets of environmental stimuli, motor requirements, and cognitive processes associated with different task phases.

Learning to ignore: a modeling study of a decremental cholinergic pathway and its influence on attention and learning.

Learning to ignore irrelevant stimuli is essential to achieving efficient and fluid attention, and serves as the complement to increasing attention to relevant stimuli. The different cholinergic (ACh) subsystems within the basal forebrain regulate attention in distinct but complementary ways. ACh projections from the substantia innominata/nucleus basalis region (SI/nBM) to the neocortex are necessary to increase attention to relevant stimuli and have been well studied. Lesser known are ACh projections from the medial septum/vertical limb of the diagonal band (MS/VDB) to the hippocampus and the cingulate that are necessary to reduce attention to irrelevant stimuli. We developed a neural simulation to provide insight into how ACh can decrement attention using this distinct pathway from the MS/VDB. We tested the model in behavioral paradigms that require decremental attention. The model exhibits behavioral effects such as associative learning, latent inhibition, and persisting behavior. Lesioning the MS/VDB disrupts latent inhibition, and drastically increases perseverative behavior. Taken together, the model demonstrates that the ACh decremental pathway is necessary for appropriate learning and attention under dynamic circumstances and suggests a canonical neural architecture for decrementing attention.

A hypothesis for temporal coding of young and mature granule cells.

While it has been hypothesized that adult neurogenesis (NG) plays a role in the encoding of temporal information at long time-scales, the temporal relationship of immature cells to the highly rhythmic network activity of the hippocampus has been largely unexplored. Here, we present a theory for how the activity of immature adult-born granule cells relates to hippocampal oscillations. Our hypothesis is that theta rhythmic (5-10 Hz) excitatory and inhibitory inputs into the hippocampus could differentially affect young and mature granule cells due to differences in intrinsic physiology and synaptic inhibition between the two cell populations. Consequently, immature cell activity may occur at broader ranges of theta phase than the activity of their mature counterparts. We describe how this differential influence on young and mature granule cells could separate the activity of differently aged neurons in a temporal coding regime. Notably, this process could have considerable implications on how the downstream CA3 region interprets the information conveyed by young and mature granule cells. To begin to investigate the phasic behavior of granule cells, we analyzed in vivo recordings of the rat dentate gyrus (DG), observing that the temporal behavior of granule cells with respect to the theta rhythm is different between rats with normal and impaired levels of NG. Specifically, in control animals, granule cells exhibit both strong and weak coupling to the phase of the theta rhythm. In contrast, the distribution of phase relationships in NG-impaired rats is shifted such that they are significantly stronger. These preliminary data support our hypothesis that immature neurons could distinctly affect the temporal dynamics of hippocampal encoding.

Simulation of cholinergic and noradrenergic modulation of behavior in uncertain environments.

Attention is a complex neurobiological process that involves rapidly and flexibly balancing sensory input and goal-directed predictions in response to environmental changes. The cholinergic and noradrenergic systems, which have been proposed to respond to expected and unexpected environmental uncertainty, respectively, play an important role in attention by differentially modulating activity in a multitude of cortical targets. Here we develop a model of an attention task that involves expected and unexpected uncertainty. The cholinergic and noradrenergic systems track this uncertainty and, in turn, influence cortical processing in five different, experimentally verified ways: (1) nicotinic enhancement of thalamocortical input, (2) muscarinic regulation of corticocortical feedback, (3) noradrenergic mediation of a network reset, (4) locus coeruleus (LC) activation of the basal forebrain (BF), and (5) cholinergic and noradrenergic balance between sensory input and frontal cortex predictions. Our results shed light on how the noradrenergic and cholinergic systems interact with each other and a distributed set of neural areas, and how this could lead to behavioral adaptation in the face of uncertainty.

Learning-dependent dynamics of beta-frequency oscillations in the basal forebrain of rats.

Cholinergic, GABAergic and glutamatergic projection neurons of the basal forebrain (BF) innervate widespread regions of the neocortex and are thought to modulate learning and attentional processes. Although it is known that neuronal cell types in the BF exhibit oscillatory firing patterns, whether the BF as a whole shows oscillatory field potential activity, and whether such neuronal patterns relate to components of cognitive tasks, has yet to be determined. To this end, local field potentials (LFPs) were recorded from the BF of rats performing an associative learning task wherein neutral objects were paired with differently valued reinforcers (pellets). Over time, rats developed preferences for the different objects based on pellet-value, indicating that the pairings had been well learned. LFPs from all rats revealed robust, short-lived bursts of beta-frequency oscillations (∼25 Hz) around the time of object encounter. Beta-frequency LFP events were found to be learning-dependent, with beta-frequency peak amplitudes significantly greater on the first day of the task when object-reinforcement pairings were novel than on the last day when pairings were well learned. The findings indicate that oscillatory bursting field potential activity occurs in the BF in freely behaving animals. Furthermore, the temporal distribution of these bursts suggests that they are probably relevant to associative learning.

Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer's disease.

Profound neuronal dysfunction in the entorhinal cortex contributes to early loss of short-term memory in Alzheimer's disease. Here we show broad neuroprotective effects of entorhinal brain-derived neurotrophic factor (BDNF) administration in several animal models of Alzheimer's disease, with extension of therapeutic benefits into the degenerating hippocampus. In amyloid-transgenic mice, BDNF gene delivery, when administered after disease onset, reverses synapse loss, partially normalizes aberrant gene expression, improves cell signaling and restores learning and memory. These outcomes occur independently of effects on amyloid plaque load. In aged rats, BDNF infusion reverses cognitive decline, improves age-related perturbations in gene expression and restores cell signaling. In adult rats and primates, BDNF prevents lesion-induced death of entorhinal cortical neurons. In aged primates, BDNF reverses neuronal atrophy and ameliorates age-related cognitive impairment. Collectively, these findings indicate that BDNF exerts substantial protective effects on crucial neuronal circuitry involved in Alzheimer's disease, acting through amyloid-independent mechanisms. BDNF therapeutic delivery merits exploration as a potential therapy for Alzheimer's disease.

Sleep deprivation in rats produces attentional impairments on a 5-choice serial reaction time task.

STUDY OBJECTIVES: To develop a rodent model of the attentional dysfunction caused by sleep loss. DESIGN: The attentional performance of rats was assessed after 4, 7, and 10 hours of total sleep deprivation on a 5-choice serial reaction time task, in which rats detect and respond to brief visual stimuli. SETTING: The rats were housed, sleep deprived, and behaviorally tested in a controlled laboratory setting. PARTICIPANTS: Ten male Long-Evans rats were used in the study. INTERVENTIONS: Rats were trained to criteria and subsequently tested in daily sessions of 100 trials at approximately 4:00 PM (lights on 8:00 AM-8:00 PM). Attentional performance was measured after 4, 7, 10 hours of total sleep deprivation induced by gentle handling. RESULTS: Sleep deprivation produced a monotonic increase in response latencies across the 4-hour, 7-hour, and 10-hour deprivations. Sleep deprivation also led to increased omission errors, but the overall number of perseverative and premature responses was unchanged. Subgroups of rats were differentially affected in the number of omission errors and perseverative responses. CONCLUSIONS: The effects of sleep deprivation on rats are compatible with a range of human findings on the effects of sleepiness on selective attention, psychomotor vigilance, and behavioral control. Rats also exhibited differential susceptibility to the effects of sleep deprivation, consistent with 'trait-like' susceptibility that has been found in humans. These findings indicate the feasibility of using the 5-choice serial reaction time task as an animal model for investigating the direct links between homeostatic sleep mechanisms and resulting attentional impairments within a single animal subject.

The basal forebrain cholinergic system is essential for cortical plasticity and functional recovery following brain injury.

A reorganization of cortical representations is postulated as the basis for functional recovery following many types of nervous system injury. Neuronal mechanisms underlying this form of cortical plasticity are poorly understood. The present study investigated the hypothesis that the basal forebrain cholinergic system plays an essential role in enabling the cortical reorganization required for functional recovery following brain injury. The results demonstrate that functional recovery following cortical injury requires basal forebrain cholinergic mechanisms and suggest that the basis for this recovery is the cholinergic-dependent reorganization of motor representations. These findings raise the intriguing possibility that deficits in cholinergic function may limit functional outcomes following nervous system injury.

Lesions of the Basal forebrain cholinergic system impair task acquisition and abolish cortical plasticity associated with motor skill learning.

The contribution of the basal forebrain cholinergic system in mediating plasticity of cortical sensorimotor representations was examined in the context of normal learning. The effects of specific basal forebrain cholinergic lesions upon cortical reorganization associated with learning a skilled motor task were investigated, addressing, for the first time, the functional consequences of blocking cortical map plasticity. Results demonstrate that disrupting basal forebrain cholinergic function disrupts cortical map reorganization and impairs motor learning. Cholinergic lesions do not impair associative fear learning or overall sensorimotor function. These results support the hypothesis that the basal forebrain cholinergic system may be specifically implicated in forms of learning requiring plasticity of cortical representations.