A neuronal network switch for approach/avoidance toggled by appetitive state

Concrete examples of computation and implementation of cost/benefit decisions at the level of neuronal circuits are largely lacking. Such decisions are based on appetitive state, which is the integration of sensation, internal state, and memory. Value-based decisions are accessible in neuronal circuitry of simple systems. In one such system, the predatory sea slug Pleurobranchaea, appetite is readily quantified in behavior and related to approach/avoidance decision. Moreover, motor aspects of feeding and turning can be observed as fictive motor output in the isolated central nervous system (CNS). Here we found that the excitation state of the feeding motor network both manifested appetitive state and controlled expression of orienting versus avoidance. In isolated CNSs, spontaneous feeding network activity varied proportionally to donor feeding thresholds. CNSs from low- and high-feeding-threshold donors expressed fictive orienting or avoidance, respectively, in response to brief stimulation of sensory nerves. Artificially exciting the feeding network converted fictive avoidance to orienting. Thus, the feeding network embodied appetitive state and toggled approach/avoidance decision by configuring response symmetry of the premotor turn network. A resulting model suggests a basic cost/benefit decision module from which to consider evolutionary elaboration of the circuitry to serve more intricate valuation processes in complex animals.     

Change in the character of directional motor reactions of female crickets <Emphasis Type="Italic">Gryllus argetinus</Emphasis> Sauss. to intraspecies signals under conditions of sensory pathology at different stages of imaginal ontogenesis

The character of motor activity of female crickets Gryllus argentinus Sauss. executing reproductive and defense behavior was studied under normal conditions and under conditions of inactivation of the cercal organ at different stages of imaginal ontogeny (on day 2, 7 and 12). Various forms of motor reactions of females placed on a movable spherical support to models of intraspecies calling and aggressive male signals were described and analyzed. Reversible inactivation of cercal receptors was shown to result in disturbance of the mechanisms of realization of normal reproductive behavior at the end of pre-reproductive and in the beginning of reproductive periods of imaginal ontogeny. It is manifested as statistically significant reduction of the proportion of positive phonotactic reactions in response to a model of the male calling song in animals with experimental sensory pathology as compared to control groups of crickets (the norm). No significant differences in proportions of typical directional motor reactions to presentation of the aggressive signal under normal conditions and under conditions of sensory pathology were found. Thus preservation of the tympanic organ was demonstrated to be a necessary but not sufficient condition for realization of adequate acoustic reproductive behavior. Only working together, distant mechanoreceptor systems (the cercal and tympanic ones) are able to provide adequacy of behavior. This conclusion confirmed the proposed earlier hypothesis about interaction of distant mechanoreceptor systems and about existence of an integrated sensory complex necessary for realization of adequate behavior of insects.     

Modeling the Impact of Lesions in the Human Brain

Lesions of anatomical brain networks result in functional disturbances of brain systems and behavior which depend sensitively, often unpredictably, on the lesion site. The availability of whole-brain maps of structural connections within the human cerebrum and our increased understanding of the physiology and large-scale dynamics of cortical networks allow us to investigate the functional consequences of focal brain lesions in a computational model. We simulate the dynamic effects of lesions placed in different regions of the cerebral cortex by recording changes in the pattern of endogenous (“resting-state”) neural activity. We find that lesions produce specific patterns of altered functional connectivity among distant regions of cortex, often affecting both cortical hemispheres. The magnitude of these dynamic effects depends on the lesion location and is partly predicted by structural network properties of the lesion site. In the model, lesions along the cortical midline and in the vicinity of the temporo-parietal junction result in large and widely distributed changes in functional connectivity, while lesions of primary sensory or motor regions remain more localized. The model suggests that dynamic lesion effects can be predicted on the basis of specific network measures of structural brain networks and that these effects may be related to known behavioral and cognitive consequences of brain lesions.     

Action and behavior: a free-energy formulation

We have previously tried to explain perceptual inference and learning under a free-energy principle that pursues Helmholtz’s agenda to understand the brain in terms of energy minimization. It is fairly easy to show that making inferences about the causes of sensory data can be cast as the minimization of a free-energy bound on the likelihood of sensory inputs, given an internal model of how they were caused. In this article, we consider what would happen if the data themselves were sampled to minimize this bound. It transpires that the ensuing active sampling or inference is mandated by ergodic arguments based on the very existence of adaptive agents. Furthermore, it accounts for many aspects of motor behavior; from retinal stabilization to goal-seeking. In particular, it suggests that motor control can be understood as fulfilling prior expectations about proprioceptive sensations. This formulation can explain why adaptive behavior emerges in biological agents and suggests a simple alternative to optimal control theory. We illustrate these points using simulations of oculomotor control and then apply to same principles to cued and goal-directed movements. In short, the free-energy formulation may provide an alternative perspective on the motor control that places it in an intimate relationship with perception.     

Change of character of directed motor reactions of female crickets Gryllus argentinus Sauss. to intraspecies signals under conditions of sensory pathology at different stages of adult ontogenesis

The character of motor activity of female crickets Gryllus argentinus Sauss. was studied in norm and under conditions of inactivation of cercal organ at realization of reproductive and protective behavior at various steps of adult ontogenesis (at the 2nd, 7th, and 12th day). There are described and analyzed various forms of female motor reactions on a movable track-ball at presentation f models of male intraspecies call and aggressive signals. The reversible inactivation or cereal receptors was shown to lead to disturbance of mechanisms of realization of normal reproductive behavior in the end of prereproductive and in the beginning of reproductive periods of adult ontogenesis. This is manifested as a significant decrease of reactions of positive phonotaxis in response to presentation of model of the male call signal in individuals with experimental sensory pathology as compared with the control cricket group (norm). No significant differences in portions of typical directed motor reactions were established in norm and under conditions of sensory pathology at presentation of aggressive signal. Thus, we have managed to show that preservation of tympanal organ is the necessary, but not sufficient condition of realization of adequate acoustic reproductive behavior. Only by working together, the distant mechanoreceptor systems (the cereal and the tympanal ones) are able to provide adequate behavior. This confirmed to earlier put forward hypothesis about interaction of distant mechanoreceptor systems and about the existence of the single sensory complex necessary for realization of insect adequate behavior.     

Converging levels of analysis in the cognitive neuroscience of visual attention.

Experiments using behavioural, lesion, functional imaging and single neuron methods are considered in the context of a neuropsychological model of visual attention. According to this model, inputs compete for representation in multiple visually responsive brain systems, sensory and motor, cortical and subcortical. Competition is biased by advance priming of neurons responsive to current behavioural targets. Across systems competition is integrated such that the same, selected object tends to become dominant throughout. The behavioural studies reviewed concern divided attention within and between modalities. They implicate within-modality competition as one main restriction on concurrent stimulus identification. In contrast to the conventional association of lateral attentional focus with parietal lobe function, the lesion studies show attentional bias to be a widespread consequence of unilateral cortical damage. Although the clinical syndrome of unilateral neglect may indeed be associated with parietal lesions, this probably reflects an assortment of further deficits accompanying a simple attentional imbalance. The functional imaging studies show joint involvement of lateral prefrontal and occipital cortex in lateral attentional focus and competition. The single unit studies suggest how competition in several regions of extrastriate cortex is biased by advance priming of neurons responsive to current behavioural targets. Together, the concepts of competition, priming and integration allow a unified theoretical approach to findings from behavioural to single neuron levels.     

Manuo-ocular coordination in target tracking. II. Comparing the model with human behavior

Several studies have shown that humans track a moving visual target with their eyes better if the movement of this target is directly controlled by the observer's hand. The improvement in performance has been attributed to coordination control between the arm motor system and the smooth pursuit (SP) system. In such a task, the SP system shows characteristics that differ from those observed during eye-alone tracking: latency (between the target-arm and the eye motion onsets) is shorter, maximum SP velocity is higher and the maximum target motion frequency at which the SP can function effectively is also higher. The aim of this article is to qualitatively evaluate the behavior of a dynamical model simulating the oculomotor system and the arm motor system when both are involved in tracking visual targets. The evaluation is essentially based on a comparison of the behavior of the model with the behavior of human subjects tracking visual targets under different conditions. The model has been introduced and quantitatively evaluated in a companion paper. The model is based on an exchange of internal information between the two sensorimotor systems, mediated by sensory signals (vision, arm muscle proprioception) and motor signals (arm motor command copy). The exchange is achieved by a specialized structure of the central nervous system, previously identified as a part of the cerebellum. Computer simulation of the model yielded results that fit the behavior of human subjects observed during previously reported experiments, both qualitatively and quantitatively. The parallelism between physiology and human behavior on the one hand, and structure and simulation of the model on the other hand, is discussed. Received: 6 March 1997 / Accepted in revised form: 15 July 1997     

Creating abstract topographic representations: Implications for coding,learning and reasoning

Topographic maps are a fundamental and ubiquitous feature of the sensory and motor regions of the brain. There is less evidence for the existence of conventional topographic maps in associational areas of the brain such as the prefrontal cortex and parietal cortex. The existence of topographically arranged anatomical projections is far more widespread and occurs in associational regions of the brain as well as sensory and motor regions: this points to a more widespread existence of topographically organised maps within associational cortex than currently recognised. Indeed, there is increasing evidence that abstract topographic representations may also occur in these regions. For example, a topographic mnemonic map of visual space has been described in the dorsolateral prefrontal cortex and topographically arranged visuospatial attentional signals have been described in parietal association cortex. This article explores how abstract representations might be extracted from sensory topographic representations and subsequently code abstract information. Finally a simple model is presented that shows how abstract topographic representations could be integrated with other information within the brain to solve problems or form abstract associations. The model uses correlative firing to detect associations between different types of stimuli. It is flexible because it can produce correlations between information represented in a topographic or non-topographic coordinate system. It is proposed that a similar process could be used in high-level cognitive operations such as learning and reasoning.     

Normalization regulates competition for visual awareness

Signals in our brain are in a constant state of competition, including those that vie for motor control, sensory dominance, and awareness. To shed light on the mechanisms underlying neural competition, we exploit binocular rivalry, a phenomenon that allows us to probe the competitive process that ordinarily transpires outside of our awareness. By measuring psychometric functions under different states of rivalry, we discovered a pattern of gain changes that are consistent with a model of competition in which attention interacts with normalization processes, thereby driving the ebb and flow between states of awareness. Moreover, we reveal that attention plays a crucial role in modulating competition; without attention, rivalry suppression for high-contrast stimuli is negligible. We propose a framework whereby our visual awareness of competing sensory representations is governed by a common neural computation: normalization.     

Org.2766 improves functional and electrophysiological aspects of regenerating sciatic nerve in the rat

The beneficial effect of short-term (8 days) melanocortin therapy on regenerating peripheral nerves is demonstrated using functional and electrophysiological tests. Following a crush lesion of the rat sciatic nerve, recovery of sensory function is monitored by assessing the responsiveness of the rat to a small electric current applied to the footsole. Recovery of motor function is assessed by means of an analysis of walking patterns. Normalization of the walking pattern reflects reinnervation of different muscle groups. The motor and H-reflex related sensory nerve conduction velocity of the regenerated nerves are longitudinally investigated in the same rats in which the recovery of motor and sensory function had been assessed previously. Functional tests show an enhanced recovery under melanocortin therapy, but in the end both saline- and melanocortin-treated rats show 100% recovery. However, when compared to the contralateral sciatic nerve, in the peptide-treated animals motor nerve conduction in the regenerated nerves has fully recovered after about 90 days following the crush lesion and the sensory conduction after about 120 days, whereas in the saline-treated rats a deficit of 20-40% in both motor and sensory conduction remains. This difference is observed even 214 days following crush.     

Analogous mechanisms compensate for neural delays in the sensory and the motor pathways: evidence from motor flash-lag

Motor behaviors require animals to coordinate neural activity across different areas within their motor system. In particular, the significant processing delays within the motor system must somehow be compensated for. Internal models of the motor system, in particular the forward model, have emerged as important potential mechanisms for compensation. For motor responses directed at moving visual objects, there is, additionally, a problem of delays within the sensory pathways carrying crucial position information. The visual phenomenon known as the flash-lag effect has led to a motion-extrapolation model for compensation of sensory delays. In the flash-lag effect, observers see a flashed item colocalized with a moving item as lagging behind the moving item. Here, we explore the possibility that the internal forward model and the motion-extrapolation model are analogous mechanisms compensating for neural delays in the motor and the visual system, respectively. In total darkness, observers moved their right hand gripping a rod while a visual flash was presented at various positions in relation to the rod. When the flash was aligned with the rod, observers perceived it in a position lagging behind the instantaneous felt position of the invisible rod. These results suggest that compensation of neural delays for time-varying motor behavior parallels compensation of delays for time-varying visual stimulation.     

A Lightweight,Headphones-based System for Manipulating Auditory Feedback in Songbirds

Experimental manipulations of sensory feedback during complex behavior have provided valuable insights into the computations underlying motor control and sensorimotor plasticity¹. Consistent sensory perturbations result in compensatory changes in motor output, reflecting changes in feedforward motor control that reduce the experienced feedback error. By quantifying how different sensory feedback errors affect human behavior, prior studies have explored how visual signals are used to recalibrate arm movements^2,3 and auditory feedback is used to modify speech production^4-7. The strength of this approach rests on the ability to mimic naturalistic errors in behavior, allowing the experimenter to observe how experienced errors in production are used to recalibrate motor output.Songbirds provide an excellent animal model for investigating the neural basis of sensorimotor control and plasticity^8,9. The songbird brain provides a well-defined circuit in which the areas necessary for song learning are spatially separated from those required for song production, and neural recording and lesion studies have made significant advances in understanding how different brain areas contribute to vocal behavior^9-12. However, the lack of a naturalistic error-correction paradigm - in which a known acoustic parameter is perturbed by the experimenter and then corrected by the songbird - has made it difficult to understand the computations underlying vocal learning or how different elements of the neural circuit contribute to the correction of vocal errors¹³.The technique described here gives the experimenter precise control over auditory feedback errors in singing birds, allowing the introduction of arbitrary sensory errors that can be used to drive vocal learning. Online sound-processing equipment is used to introduce a known perturbation to the acoustics of song, and a miniaturized headphones apparatus is used to replace a songbird''s natural auditory feedback with the perturbed signal in real time. We have used this paradigm to perturb the fundamental frequency (pitch) of auditory feedback in adult songbirds, providing the first demonstration that adult birds maintain vocal performance using error correction¹⁴. The present protocol can be used to implement a wide range of sensory feedback perturbations (including but not limited to pitch shifts) to investigate the computational and neurophysiological basis of vocal learning.     

Independent development of sensory and motor innervation patterns in embryonic chick hindlimbs

Previous studies suggest that sensory axon outgrowth is guided by motoneurons, which are specified to innervate particular target muscles. Here we present evidence that questions this conclusion. We have used a new approach to assess the pathfinding abilities of bona fide sensory neurons, first by eliminating motoneurons after neural crest cells have coalesced into dorsal root ganglia (DRG) and second by challenging sensory neurons to innervate muscles in a novel environment created by shifting a limb bud rostrally. The resulting sensory innervation patterns mapped with the lipophilic dyes DiI and DiA showed that sensory axons projected robustly to muscles in the absence of motoneurons, if motoneurons were eliminated after DRG formation. Moreover, sensory neurons projected appropriately to their usual target muscles under these conditions. In contrast, following limb shifts, muscle sensory innervation was often derived from inappropriate segments. In this novel environment, sensory neurons tended to make more "mistakes" than motoneurons. Whereas motoneurons tended to innervate their embryologically correct muscles, sensory innervation was more widespread and was generally from more rostral segments than normal. Similar results were obtained when motoneurons were eliminated in embryos with limb shifts. These findings show that sensory neurons are capable of navigating through their usual terrain without guidance from motor axons. However, unlike motor axons, sensory axons do not appear to actively seek out appropriate target muscles when confronted with a novel terrain. These findings suggest that sensory neuron identity with regard to pathway and target choice may be unspecified or quite plastic at the time of initial axon outgrowth.     

Segmental motion of forefoot and hindfoot as a diagnostic tool

Segmental motions derived from non-invasive motion analysis are being used to investigate the intrinsic functional behavior of the foot and ankle in health and disease. The goal of this research was to examine the ability of a generic segmented model of the foot to capture and differentiate changes in internal skeletal kinematics due to neuromuscular disease and/or trauma. A robotic apparatus that reproduces the kinematics and kinetics of gait in cadaver lower extremities was employed to produce motion under normal and aberrant neuromuscular activation patterns of tibialis posterior and/or tibialis anterior. Stance phase simulations were conducted on 10 donor limbs while recording three-dimensional kinematic trajectories of (1) skin-mounted markers used clinically to construct segmented foot models, and (2) bone-mounted marker clusters to capture actual internal bone motion as the gold standard for comparison. The models constructed from external marker data were able to differentiate the kinematic behaviors elicited by different neuromuscular conditions in a manner similar to that using the bone-derived data. Measurable differences between internal and externally measured kinematics were small, variable and random across the three axes of rotation and neuromuscular conditions, with a tendency toward more differences noted during early and late stance. Albeit slightly different, three-dimensional motion profiles of the hindfoot and forefoot segments correlated well with internal skeletal motion under all neuromuscular conditions, thereby confirming the utility of measuring segmental motions as a valid means of clinical assessment.     

Target-dependent morphological segregation of Aplysia sensory outgrowth in vitro.

The adult nervous system is characterized by partial or complete morphological segregation of terminals from different afferent neurons innervating the same postsynaptic target. This segregation is thought to result, in part, from competition between the afferent terminals. To explore the role of the target cell in the spatial distribution of presynaptic inputs, the sensory neurons of Aplysia were cultured either with or without a common target motor neuron. In the presence of a common target, the outgrowth from two different sensory neurons tends to occupy separate postsynaptic regions. When cultured without a target motor neuron, processes from different sensory neurons do not segregate, but rather grow freely along one another. Thus, morphological segregation of sensory outgrowth requires interaction with a target neuron and may reflect competition between presynaptic terminals for a limited number of synaptic sites on the motor neuron, or for a postsynaptic trophic factor.     

Schema-based learning of adaptable and flexible prey-catching in anurans I. The basic architecture

A motor action often involves the coordination of several motor synergies and requires flexible adjustment of the ongoing execution based on feedback signals. To elucidate the neural mechanisms underlying the construction and selection of motor synergies, we study prey-capture in anurans. Experimental data demonstrate the intricate interaction between different motor synergies, including the interplay of their afferent feedback signals (Weerasuriya 1991; Anderson and Nishikawa 1996). Such data provide insights for the general issues concerning two-way information flow between sensory centers, motor circuits and periphery in motor coordination. We show how different afferent feedback signals about the status of the different components of the motor apparatus play a critical role in motor control as well as in learning. This paper, along with its companion paper, extend the model by Liaw et al. (1994) by integrating a number of different motor pattern generators, different types of afferent feedback, as well as the corresponding control structure within an adaptive framework we call Schema-Based Learning. We develop a model of the different MPGs involved in prey-catching as a vehicle to investigate the following questions: What are the characteristic features of the activity of a single muscle? How can these features be controlled by the premotor circuit? What are the strategies employed to generate and synchronize motor synergies? What is the role of afferent feedback in shaping the activity of a MPG? How can several MPGs share the same underlying circuitry and yet give rise to different motor patterns under different input conditions? In the companion paper we also extend the model by incorporating learning components that give rise to more flexible, adaptable and robust behaviors. To show these aspects we incorporate studies on experiments on lesions and the learning processes that allow the animal to recover its proper functioning     

Diversity in mating behavior of hermaphroditic and male-female Caenorhabditis nematodes

In this study, we addressed why Caenorhabditis elegans males are inefficient at fertilizing their hermaphrodites. During copulation, hermaphrodites generally move away from males before they become impregnated. C. elegans hermaphrodites reproduce by internal self-fertilization, so that copulation with males is not required for species propagation. The hermaphroditic mode of reproduction could potentially relax selection for genes that optimize male mating behavior. We examined males from hermaphroditic and gonochoristic (male-female copulation) Caenorhabditis species to determine if they use different sensory and motor mechanisms to control their mating behavior. Instead, we found through laser ablation analysis and behavioral observations that hermaphroditic C. briggsae and gonochoristic C. remanei and Caenorhabditis species 4, PB2801 males produce a factor that immobilizes females during copulation. This factor also stimulates the vulval slit to widen, so that the male copulatory spicules can easily insert. C. elegans and C. briggsae hermaphrodites are not affected by this factor. We suggest that sensory and motor execution of mating behavior have not significantly changed among males of different Caenorhabditis species; however, during the evolution of internal self-fertilization, hermaphrodites have lost the ability to respond to the male soporific-inducing factor.     

Learning the dynamics of reaching movements results in the modification of arm impedance and long-latency perturbation responses

 Some characteristics of arm movements that humans exhibit during learning the dynamics of reaching are consistent with a theoretical framework where training results in motor commands that are gradually modified to predict and compensate for novel forces that may act on the hand. As a first approximation, the motor control system behaves as an adapting controller that learns an internal model of the dynamics of the task. It approximates inverse dynamics and predicts motor commands that are appropriate for a desired limb trajectory. However, we had previously noted that subtle motion characteristics observed during changes in task dynamics challenged this simple model and raised the possibility that adaptation also involved sensory–motor feedback pathways. These pathways reacted to sensory feedback during the course of the movement. Here we hypothesize that adaptation to dynamics might also involve a modification of how the CNS responds to sensory feedback. We tested this through experiments that quantified how the motor system's response to errors during voluntary movements changed as it adapted to dynamics of a force field. We describe a nonlinear approach that approximates the impedance of the arm, i.e., force response as a function of arm displacement trajectory. We observe that after adaptation, the impedance function changes in a way that closely matches and counters the effect of the force field. This is particularly prominent in the long-latency (>100 ms) component of response to perturbations. Therefore, it appears that practice not only modifies the internal model with which the brain generates motor commands that initiate a movement, but also the internal model with which sensory feedback is integrated with the ongoing descending commands in order to respond to error during the movement. Received: 10 January 2001 / Accepted in revised form: 30 May 2001     

Optimality in mono- and multisensory map formation

In the struggle for survival in a complex and dynamic environment, nature has developed a multitude of sophisticated sensory systems. In order to exploit the information provided by these sensory systems, higher vertebrates reconstruct the spatio-temporal environment from each of the sensory systems they have at their disposal. That is, for each modality the animal computes a neuronal representation of the outside world, a monosensory neuronal map. Here we present a universal framework that allows to calculate the specific layout of the involved neuronal network by means of a general mathematical principle, viz., stochastic optimality. In order to illustrate the use of this theoretical framework, we provide a step-by-step tutorial of how to apply our model. In so doing, we present a spatial and a temporal example of optimal stimulus reconstruction which underline the advantages of our approach. That is, given a known physical signal transmission and rudimental knowledge of the detection process, our approach allows to estimate the possible performance and to predict neuronal properties of biological sensory systems. Finally, information from different sensory modalities has to be integrated so as to gain a unified perception of reality for further processing, e.g., for distinct motor commands. We briefly discuss concepts of multimodal interaction and how a multimodal space can evolve by alignment of monosensory maps.     

Comparative approaches to avian song system function: insights into auditory and motor processing

Many fundamental advances in our understanding of basic neural function have been made using bird song learning and performance as a model system. These advances have included a greater understanding of higher-order neural processing, developmental and hormonal influences on behavior, and the realization that neurogenesis plays an important role in normal adult brain function. The great diversity of passerine birds and song-related behaviors they exhibit suggest that oscine songbirds are ideally suited for comparative studies. While the comparative approach has been used successfully in the past to study song-related phenomena at anatomical and behavioral levels, it has been underutilized in addressing questions at the neurophysiological level. Most neurophysiological studies of songbird auditory and motor processing have been performed in one species, the zebra finch (Taeniopygia guttata). We present and compare neurophysiological studies we have performed in zebra finches and song sparrows (Melospiza melodia), species that differ markedly in their singing behavior and song repertoire characteristics. Interspecific similarities, and striking differences, in song neural processing are apparent. While preliminary, these data suggest that comparative neurophysiological studies of species carefully chosen for their vocal repertoire and singing behavior will contribute significantly to our understanding of vertebrate sensory and motor neural processing.