Spatial gradients and multidimensional dynamics in a neural integrator circuit

Princeton Neuroscience Institute and Department of Molecular Biology, Princeton University, Princeton, New Jersey, USA.
Nature Neuroscience (Impact Factor: 16.1). 08/2011; 14(9):1150-9. DOI: 10.1038/nn.2888
Source: PubMed


In a neural integrator, the variability and topographical organization of neuronal firing-rate persistence can provide information about the circuit's functional architecture. We used optical recording to measure the time constant of decay of persistent firing (persistence time) across a population of neurons comprising the larval zebrafish oculomotor velocity-to-position neural integrator. We found extensive persistence time variation (tenfold; coefficients of variation = 0.58-1.20) across cells in individual larvae. We also found that the similarity in firing between two neurons decreased as the distance between them increased and that a gradient in persistence time was mapped along the rostrocaudal and dorsoventral axes. This topography is consistent with the emergence of persistence time heterogeneity from a circuit architecture in which nearby neurons are more strongly interconnected than distant ones. Integrator circuit models characterized by multiple dimensions of slow firing-rate dynamics can account for our results.

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Available from: Aristides Arrenberg, Mar 07, 2014
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    • "Such results were interpreted to suggest the presence of neural integrators in the circuit, as velocity signals can be integrated to yield position signals (Robinson, 1989; Miri et al., 2011). Our finding that most sensorimotor striatal neurons are correlated with velocity suggests the possibility that a neural integrator is found in the basal ganglia circuitry. "
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    ABSTRACT: Although the basal ganglia have long been implicated in the initiation of actions, their contribution to movement remains a matter of dispute. Using wireless multi-electrode recording and motion tracking, we examined the relationship between single-unit activity in the sensorimotor striatum and movement kinematics. We recorded single-unit activity from medium spiny projection neurons and fast-spiking interneurons while monitoring the movements of mice using motion tracking. In Experiment 1, we trained mice to generate movements reliably by water-depriving them and giving them periodic cued sucrose rewards. We found high correlations between single-unit activity and movement velocity in particular directions. This correlation was found in both putative medium spiny projection neurons and fast-spiking interneurons. In Experiment 2, to rule out the possibility that the observed correlations were due to reward expectancy, we repeated the same procedure but added trials in which sucrose delivery was replaced by an aversive air puff stimulus. The air puff generated avoidance movements that were clearly different from movements on rewarded trials, but the same neurons that showed velocity correlation on reward trials exhibited a similar correlation on air puff trials. These experiments show for the first time that the firing rate of striatal neurons reflects movement velocity for different types of movements, whether to seek rewards or to avoid harm.
    European Journal of Neuroscience 09/2014; 40(10). DOI:10.1111/ejn.12722 · 3.18 Impact Factor
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    • "It now is possible to go beyond the traditional approaches used in monkey research, and to answer questions that were intractable in the past. For example, imaging of calcium signals makes it possible to record from many nearby neurons simultaneously with a temporal resolution that is good enough to capture the relationships between neural and behavioral or stimulus dynamics (Stosiek et al., 2003; Rothschild et al., 2010; Miri et al., 2011). Activation of specific subpopulations of neurons through optogenetics provides a carefully controlled tool for dissection of neural circuits in behaving animals (Han and Boyden, 2007). "
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    ABSTRACT: Selection of a model organism creates a tension between competing constraints. The recent explosion of modern molecular techniques has revolutionized the analysis of neural systems in organisms that are amenable to genetic techniques. Yet, the non-human primate remains the gold-standard for the analysis of the neural basis of behavior, and as a bridge to the operation of the human brain. The challenge is to generalize across species in a way that exposes the operation of circuits as well as the relationship of circuits to behavior. Eye movements provide an opportunity to cross the bridge from mechanism to behavior through research on diverse species. Here, we review experiments and computational studies on a circuit function called "neural integration" that occurs in the brainstems of larval zebrafish, non-human primates, and species "in between". We show that analysis of circuit structure using modern molecular and imaging approaches in zebrafish has remarkable explanatory power for the details of the responses of integrator neurons in the monkey. The combination of research from the two species has led to a much stronger hypothesis for the implementation of the neural integrator than could have been achieved using either species alone.
    Neuroscience 05/2014; 296. DOI:10.1016/j.neuroscience.2014.04.048 · 3.36 Impact Factor
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    • "The photoactivated volumes were columns of tissue approximately 10–15 cells wide and protruding through the entire dorsoventral extent of the hindbrain, as judged by Kaede photoconversion experiments (Figure A7). The maximal effect was observed around 50–150 μm caudal of the Mauthner cells, somewhat more rostral (rhombomere 5, 6, and 7) than in the previous reports (Miri et al., 2011a,b) (Figure 4D, Supplementary Movie 1). "
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    ABSTRACT: Many neural systems can store short-term information in persistently firing neurons. Such persistent activity is believed to be maintained by recurrent feedback among neurons. This hypothesis has been fleshed out in detail for the oculomotor integrator (OI) for which the so-called "line attractor" network model can explain a large set of observations. Here we show that there is a plethora of such models, distinguished by the relative strength of recurrent excitation and inhibition. In each model, the firing rates of the neurons relax toward the persistent activity states. The dynamics of relaxation can be quite different, however, and depend on the levels of recurrent excitation and inhibition. To identify the correct model, we directly measure these relaxation dynamics by performing optogenetic perturbations in the OI of zebrafish expressing halorhodopsin or channelrhodopsin. We show that instantaneous, inhibitory stimulations of the OI lead to persistent, centripetal eye position changes ipsilateral to the stimulation. Excitatory stimulations similarly cause centripetal eye position changes, yet only contralateral to the stimulation. These results show that the dynamics of the OI are organized around a central attractor state-the null position of the eyes-which stabilizes the system against random perturbations. Our results pose new constraints on the circuit connectivity of the system and provide new insights into the mechanisms underlying persistent activity.
    Frontiers in Neural Circuits 02/2014; 8:10. DOI:10.3389/fncir.2014.00010 · 3.60 Impact Factor
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