Gene networks activated by specific patterns of action potentials in dorsal root ganglia neurons

Lee, Philip R.; Cohen, Jeffrey K.; Iacobaş, Dumitru A.; Iacobaş, Sanda; Fields, R. Douglas

doi:10.1038/srep43765

Cited by 55 publications

(75 citation statements)

References 52 publications

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“…PSINA, by orchestrating cellular communication at temporal and spatial scales inaccessible to other signaling mechanisms, may be acting to refine this first draft to complete the self-assembly of the brain. Sweeps of activity repeatedly coursing through the brain through different ‘channels’ could link distinct sets of neurons to direct coordinated morphological changes and sculpt cell-cell contacts, strengthen synapses with correct targets while weakening and pruning incorrect pairings, and control transcription programs that direct circuit refinement (Lee et al, 2017; Nakashima et al, 2013; Serizawa et al, 2006; Tyssowski et al, 2018). PSINA may act as a ‘dress rehearsal’ for neural networks, preparing for ‘opening night’ at the completion of development.…”

Section: Discussionmentioning

confidence: 99%

Cell-type specific patterned stimulus-independent neuronal activity in theDrosophilavisual system during synapse formation

Akin

Bajar

Keleş

et al. 2018

Preprint

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16Stereotyped synaptic connections define the neural circuits of the brain. In vertebrates, stimulus-independent 17 activity contributes to neural circuit formation. It is unknown whether this type of activity is a general feature of 18 nervous system development. Here, we report patterned, stimulus-independent neural activity in the Drosophila 19 visual system during synaptogenesis. Using in vivo calcium, voltage, and glutamate imaging, we found that all 20 neurons participate in this spontaneous activity, which is characterized by brain-wide periodic active and silent 21 phases. Glia are active in a complementary pattern. Each of the 15 examined of the over 100 specific neuron 22 types in the fly visual system exhibited a unique activity signature. The activity of neurons that are synaptic 23 partners in the adult was highly correlated during development. We propose that this cell type-specific activity 24 coordinates the development of the functional circuitry of the adult brain. 25 26 Keywords 27 Nervous system development, visual system development, neuronal activity, synaptogenesis, calcium imaging, 28 2-photon microscopy. 29 30 42superior colliculus (SC), and the visual cortex (Ackman et al., 2012). In each of these areas, large populations of 43 neighboring cells exhibit correlated firing patterns. Significant progress has been made toward characterizing 44 and identifying the organizing principles of spontaneous activity in the developing vertebrate brain, and the 45 precise developmental role of this activity is an area of active interest. 46 By contrast to vertebrates, brain development in invertebrates is thought to be driven by hardwired 47 48 dependent neural activity. Previous work has shown that, in the Drosophila visual system, photoreceptor 49 3 neurons can develop the wild-type complement of synapses in a stimulus-independent manner (Hiesinger et al., 50 2006). However, the existence and significance of spontaneous activity during invertebrate brain development 51 remains an open question. 52 Some of the most detailed understanding of brain development in the fly comes from the visual system. 53 Visual information from the compound eye is relayed in a topographic fashion to the optic neuropils-the 54 lamina, medulla, and the lobula complex. These neuropils are organized into columns and layers. In general, 55 columns process information from different points in visual space, and layers process different types of visual 56 information. Over 100 different neuronal cell types form precise synaptic connections, typically with several 57 different cell types. The three dimensional EM re-constructions of the optic neuropils that reveal this wiring 58 complexity (Rivera-Alba et al., 2011; Takemura et al., 2013 Takemura et al., , 2017 also underscore the challenge of 59 understanding the mechanisms of synaptic specificity: Most neurons make synapses with only a subset of their 60 contact neighbors, and the area of contact has little bearing on this decision. 61 Vis...

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Section: Discussionmentioning

confidence: 99%

Cell-type specific patterned stimulus-independent neuronal activity in theDrosophilavisual system during synapse formation

Akin

Bajar

Keleş

et al. 2018

Preprint

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“…Moreover, even for a single cell type, a given physiological or behavioral context may result in different patterns of spatiotemporal input to the cell, and there is some evidence that this could affect different subsets of genes. Direct evidence for sensitivity to stimulus structure comes from recent studies of cultured neurons, where different temporal patterns of electrical or chemical depolarization were found to trigger different gene response patterns (18,19). Within the brain, where neurons are synaptically connected, gAPs induced by somatic calcium influx (i.e., neuronal firing) may differ from ones driven by localized dendritic activity (see below).…”

Section: Gap In the Cell: Molecular Elementsmentioning

confidence: 99%

The role of the genome in experience-dependent plasticity: Extending the analogy of the genomic action potential

Clayton

Anreiter

Aristizabal

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Our past experiences shape our current and future behavior. These experiences must leave some enduring imprint on our brains, altering neural circuits that mediate behavior and contributing to our individual differences. As a framework for understanding how experiences might produce lasting changes in neural circuits, Clayton [D. F. Clayton, Neurobiol. Learn. Mem. 74, 185–216 (2000)] introduced the concept of the genomic action potential (gAP)—a structured genomic response in the brain to acute experience. Similar to the familiar electrophysiological action potential (eAP), the gAP also provides a means for integrating afferent patterns of activity but on a slower timescale and with longer-lasting effects. We revisit this concept in light of contemporary work on experience-dependent modification of neural circuits. We review the “Immediate Early Gene” (IEG) response, the starting point for understanding the gAP. We discuss evidence for its involvement in the encoding of experience to long-term memory across time and biological levels of organization ranging from individual cells to cell ensembles and whole organisms. We explore distinctions between memory encoding and homeostatic functions and consider the potential for perpetuation of the imprint of experience through epigenetic mechanisms. We describe a specific example of a gAP in humans linked to individual differences in the response to stress. Finally, we identify key objectives and new tools for continuing research in this area.

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“…As well, patterns of activity-dependent gene expression are also sensitive to the temporal pattern of activity. The same number of stimuli delivered in two different temporal patterns resulted in differential expression of activity-dependent genes [•Lee et al 2017]. As well, the temporal pattern of stimulation can also influence non-neural cells.…”

Section: Resultsmentioning

confidence: 99%

Temporal pattern of electrical stimulation is a new dimension of therapeutic innovation

Grill

2018

Current Opinion in Biomedical Engineering

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Artificial activation of the nervous system requires selection of appropriate stimulation parameters including stimulation amplitude, stimulation pulse duration, and stimulation pulse repetition rate. The temporal pattern of stimulation, i.e., the timing between stimulation pulses, is a novel dimension of stimulation parameter tuning. The effects evoked by artificial activation of the nervous system are dependent on the pattern of stimulation, and different patterns of stimulation, even when delivered at the same average rate, evoke different functional effects, different changes in synaptic plasticity, and even different patterns of gene expression. Non-regular temporal patterns of stimulation offer the opportunity to improve the efficacy and efficiency of therapeutic stimulation as well as to manipulate other processes in the nervous system. The potential design space for sequences of varying interpulse intervals is exceedingly large and sound approaches to design stimulation patterns are required as an empirical approach is not practical.

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Gene networks activated by specific patterns of action potentials in dorsal root ganglia neurons

Cited by 55 publications

References 52 publications

Cell-type specific patterned stimulus-independent neuronal activity in theDrosophilavisual system during synapse formation

Cell-type specific patterned stimulus-independent neuronal activity in theDrosophilavisual system during synapse formation

The role of the genome in experience-dependent plasticity: Extending the analogy of the genomic action potential

Temporal pattern of electrical stimulation is a new dimension of therapeutic innovation

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