Transformation of context-dependent sensory dynamics into motor behavior

Latorre R, Levi R, Varona P (2013) Transformation of Context-dependent Sensory Dynamics into Motor Behavior. PLoS Comput Biol 9(2): e1002908. doi:10.1371/journal.pcbi.1002908The intrinsic dynamics of sensory networks play an important role in the sensory-motor transformation. In this paper we use conductance based models and electrophysiological recordings to address the study of the dual role of a sensory network to organize two behavioral context-dependent motor programs in the mollusk Clione limacina. We show that: (i) a winner take-all dynamics in the gravimetric sensory network model drives the typical repetitive rhythm in the wing central pattern generator (CPG) during routine swimming; (ii) the winnerless competition dynamics of the same sensory network organizes the irregular pattern observed in the wing CPG during hunting behavior. Our model also shows that although the timing of the activity is irregular, the sequence of the switching among the sensory cells is preserved whenever the same set of neurons are activated in a given time window. These activation phase locks in the sensory signals are transformed into specific events in the motor activity. The activation phase locks can play an important role in motor coordination driven by the intrinsic dynamics of a multifunctional sensory organThis work was supported by MINECO TIN2012-30883 and IPT-2011-0727-020000

Involvement of the cortico-basal ganglia-thalamocortical loop in developmental stuttering

Stuttering is a complex neurodevelopmental disorder that has to date eluded a clear explication of its pathophysiological bases. In this review, we utilize the Directions Into Velocities of Articulators (DIVA) neurocomputational modeling framework to mechanistically interpret relevant findings from the behavioral and neurological literatures on stuttering. Within this theoretical framework, we propose that the primary impairment underlying stuttering behavior is malfunction in the cortico-basal ganglia-thalamocortical (hereafter, cortico-BG) loop that is responsible for initiating speech motor programs. This theoretical perspective predicts three possible loci of impaired neural processing within the cortico-BG loop that could lead to stuttering behaviors: impairment within the basal ganglia proper; impairment of axonal projections between cerebral cortex, basal ganglia, and thalamus; and impairment in cortical processing. These theoretical perspectives are presented in detail, followed by a review of empirical data that make reference to these three possibilities. We also highlight any differences that are present in the literature based on examining adults versus children, which give important insights into potential core deficits associated with stuttering versus compensatory changes that occur in the brain as a result of having stuttered for many years in the case of adults who stutter. We conclude with outstanding questions in the field and promising areas for future studies that have the potential to further advance mechanistic understanding of neural deficits underlying persistent developmental stuttering.R01 DC007683 - NIDCD NIH HHS; R01 DC011277 - NIDCD NIH HHSPublished versio

On the notion of motor primitives in humans and robots

This article reviews two reflexive motor patterns in humans: Primitive reflexes and motor primitives. Both terms coexist in the literature of motor development and motor control, yet they are not synonyms. While primitive reflexes are a part of the temporary motor repertoire in early ontogeny, motor primitives refer to sets of motor patterns that are considered basic units of voluntary motor control thought to be present throughout the life-span. The article provides an overview of the anatomy and neurophysiology of human reflexive motor patterns to elucidate that both concepts are rooted in architecture of the spinal cord. I will advocate that an understanding of the human motor system that encompasses both primitive reflexes and motor primitives as well as the interaction with supraspinal motor centers will lead to an appreciation of the richness of the human motor repertoire, which in turn seems imperative for designing epigenetic robots and highly adaptable human machine interfaces

Robust dynamical invariants in sequential neural activity

By studying different sources of temporal variability in central pattern generator (CPG) circuits, we unveil fundamental aspects of the instantaneous balance between flexibility and robustness in sequential dynamics -a property that characterizes many systems that display neural rhythms. Our analysis of the triphasic rhythm of the pyloric CPG (Carcinus maenas) shows strong robustness of transient dynamics in keeping not only the activation sequences but also specific cycle-by-cycle temporal relationships in the form of strong linear correlations between pivotal time intervals, i.e. dynamical invariants. The level of variability and coordination was characterized using intrinsic time references and intervals in long recordings of both regular and irregular rhythms. Out of the many possible combinations of time intervals studied, only two cycle-by-cycle dynamical invariants were identified, existing even outside steady states. While executing a neural sequence, dynamical invariants reflect constraints to optimize functionality by shaping the actual intervals in which activity emerges to build the sequence. Our results indicate that such boundaries to the adaptability arise from the interaction between the rich dynamics of neurons and connections. We suggest that invariant temporal sequence relationships could be present in other networks, including those shaping sequences of functional brain rhythms, and underlie rhythm programming and functionalityThis work has been supported by Spanish grants MINECO DPI2015-65833-P, TIN2017-84452-R, PGC2018-095895-B-I00 (http:// www.mineco.gob.es/), and ONRG grant N62909-14-1-N279

Analytical CPG model driven by limb velocity input generates accurate temporal locomotor dynamics

The ability of vertebrates to generate rhythm within their spinal neural networks is essential for walking, running, and other rhythmic behaviors. The central pattern generator (CPG) network responsible for these behaviors is well-characterized with experimental and theoretical studies, and it can be formulated as a nonlinear dynam- ical system. The underlying mechanism responsible for locomotor behavior can be expressed as the process of leaky integration with resetting states generating appropriate phases for changing body velocity. The low-dimensional input to the CPG model generates the bilateral pattern of swing and stance modulation for each limb and is consistent with the desired limb speed as the input command. To test the minimal configuration of required parameters for this model, we reduced the system of equations representing CPG for a single limb and provided the analytical solution with two complementary methods. The analytical and empirical cycle durations were similar (R2 = 0.99) for the full range of walking speeds. The structure of solution is consistent with the use of limb speed as the input domain for the CPG network. Moreover, the reciprocal interaction between two leaky integration processes representing a CPG for two limbs was sufficient to capture fundamental experimental dynamics associated with the control of heading direction. This analysis provides further support for the embedded velocity or limb speed representation within spinal neural pathways involved in rhythm generation

Neural dynamics of social behavior : An evolutionary and mechanistic perspective on communication, cooperation, and competition among situated agents

Social behavior can be found on almost every level of life, ranging from microorganisms to human societies. However, explaining the evolutionary emergence of cooperation, communication, or competition still challenges modern biology. The most common approaches to this problem are based on game-theoretic models. The problem is that these models often assume fixed and limited rules and actions that individual agents can choose from, which excludes the dynamical nature of the mechanisms that underlie the behavior of living systems. So far, there exists a lack of convincing modeling approaches to investigate the emergence of social behavior from a mechanistic and evolutionary perspective. Instead of studying animals, the methodology employed in this thesis combines several aspects from alternative approaches to study behavior in a rather novel way. Robotic models are considered as individual agents which are controlled by recurrent neural networks representing non-linear dynamical system. The topology and parameters of these networks are evolved following an open-ended evolution approach, that is, individuals are not evaluated on high-level goals or optimized for specific functions. Instead, agents compete for limited resources to enhance their chance of survival. Further, there is no restriction with respect to how individuals interact with their environment or with each other. As its main objective, this thesis aims at a complementary approach for studying not only the evolution, but also the mechanisms of basic forms of communication. For this purpose it can be shown that a robot does not necessarily have to be as complex as a human, not even as complex as a bacterium. The strength of this approach is that it deals with rather simple, yet complete and situated systems, facing similar real world problems as animals do, such as sensory noise or dynamically changing environments. The experimental part of this thesis is substantiated in a five-part examination. First, self-organized aggregation patterns are discussed. Second, the advantages of evolving decentralized control with respect to behavioral robustness and flexibility is demonstrated. Third, it is shown that only minimalistic local acoustic communication is required to coordinate the behavior of large groups. This is followed by investigations of the evolutionary emergence of communication. Finally, it is shown how already evolved communicative behavior changes during further evolution when a population is confronted with competition about limited environmental resources. All presented experiments entail thorough analysis of the dynamical mechanisms that underlie evolved communication systems, which has not been done so far in the context of cooperative behavior. This framework leads to a better understanding of the relation between intrinsic neurodynamics and observable agent-environment interactions. The results discussed here provide a new perspective on the evolution of cooperation because they deal with aspects largely neglected in traditional approaches, aspects such as embodiment, situatedness, and the dynamical nature of the mechanisms that underlie behavior. For the first time, it can be demonstrated how noise influences specific signaling strategies and that versatile dynamics of very small-scale neural networks embedded in sensory-motor feedback loops give rise to sophisticated forms of communication such as signal coordination, cooperative intraspecific communication, and, most intriguingly, aggressive interspecific signaling. Further, the results demonstrate the development of counteractive niche construction based on a modification of communication strategies which generates an evolutionary feedback resulting in an active reduction of selection pressure, which has not been shown so far. Thus, the novel findings presented here strongly support the complementary nature of robotic experiments to study the evolution and mechanisms of communication and cooperation.</p

Duets recorded in the wild reveal that interindividually coordinated motor control enables cooperative behavior

Many organisms coordinate rhythmic motor actions with those of a partner to generate cooperative social behavior such as duet singing. The neural mechanisms that enable rhythmic interindividual coordination of motor actions are unknown. Here we investigate the neural basis of vocal duetting behavior by using an approach that enables simultaneous recordings of individual vocalizations and multiunit vocal premotor activity in songbird pairs ranging freely in their natural habitat. We find that in the duet-initiating bird, the onset of the partner's contribution to the duet triggers a change in rhythm in the periodic neural discharges that are exclusively locked to the initiating bird's own vocalizations. The resulting interindividually synchronized neural activity pattern elicits vocalizations that perfectly alternate between partners in the ongoing song. We suggest that rhythmic cooperative behavior requires exact interindividual coordination of premotor neural activity, which might be achieved by integration of sensory information originating from the interacting partner

Identification of a rhythmic firing pattern in the enteric nervous system that generates rhythmic electrical activity in smooth muscle

The enteric nervous system (ENS) contains millions of neurons essential for organization of motor behavior of the intestine. It is well established that the large intestine requires ENS activity to drive propulsive motor behaviors. However, the firing pattern of the ENS underlying propagating neurogenic contractions of the large intestine remains unknown. To identify this, we used high-resolution neuronal imaging with electrophysiology from neighboring smooth muscle. Myoelectric activity underlying propagating neurogenic contractions along murine large intestine [also referred to as colonic migrating motor complexes, (CMMCs)] consisted of prolonged bursts of rhythmic depolarizations at a frequency of ∼2 Hz. Temporal coordination of this activity in the smooth muscle over large spatial fields (∼7 mm, longitudinally) was dependent on the ENS. During quiescent periods between neurogenic contractions, recordings from large populations of enteric neurons, in mice of either sex, revealed ongoing activity. The onset of neurogenic contractions was characterized by the emergence of temporally synchronized activity across large populations of excitatory and inhibitory neurons. This neuronal firing pattern was rhythmic and temporally synchronized across large numbers of ganglia at ∼2 Hz. ENS activation preceded smooth muscle depolarization, indicating rhythmic depolarizations in smooth muscle were controlled by firing of enteric neurons. The cyclical emergence of temporally coordinated firing of large populations of enteric neurons represents a unique neural motor pattern outside the CNS. This is the first direct observation of rhythmic firing in the ENS underlying rhythmic electrical depolarizations in smooth muscle. The pattern of neuronal activity we identified underlies the generation of CMMCs

Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva

This is the final version of the article. Available from the publisher via the DOI in this record.Ciliated surfaces harbouring synchronously beating cilia can generate fluid flow or drive locomotion. In ciliary swimmers, ciliary beating, arrests, and changes in beat frequency are often coordinated across extended or discontinuous surfaces. To understand how such coordination is achieved, we studied the ciliated larvae of Platynereis dumerilii, a marine annelid. Platynereis larvae have segmental multiciliated cells that regularly display spontaneous coordinated ciliary arrests. We used whole-body connectomics, activity imaging, transgenesis, and neuron ablation to characterize the ciliomotor circuitry. We identified cholinergic, serotonergic, and catecholaminergic ciliomotor neurons. The synchronous rhythmic activation of cholinergic cells drives the coordinated arrests of all cilia. The serotonergic cells are active when cilia are beating. Serotonin inhibits the cholinergic rhythm, and increases ciliary beat frequency. Based on their connectivity and alternating activity, the catecholaminergic cells may generate the rhythm. The ciliomotor circuitry thus constitutes a stop-and-go pacemaker system for the whole-body coordination of ciliary locomotion.The research leading to these results received funding from the European Research Council under the European Union’s Seventh Framework Programme (FP7/2007-2013)/European Research Council Grant Agreement 260821. This project is supported by the Marie Curie ITN ‘Neptune’, GA 317172, funded under the FP7, PEOPLE Work Programme of the European Commission. This project is supported by the DFG - Deutsche Forschungsgemeinschaft (Reference no. JE 777/3–1).Deutsche Forschungsgemeinschaft 777/3-1 Gaspar JekelyMax-Planck-Gesellschaft Open-access funding Gaspar JekelyEuropean Commission GA 317172 Gaspar Jekel