Closing the gap: long-term presynaptic plasticity in brain function and disease

Monday, Hannah R.; Castillo, Pablo E.

doi:10.1016/j.conb.2017.05.011

Cited by 50 publications

(47 citation statements)

References 79 publications

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“…Our results suggest that by altering the balance of multiple transmitters with opposing actions, a single presynaptic neuron can evoke excitatory and inhibitory postsynaptic responses, convey the valence information of sensory stimulus to the circuit, and induce an appropriate behavior. Our observations provide a sharp contrast to current views of presynaptic plasticity, in which presynaptic regulation facilitates or depresses the strength of the postsynaptic response 63,64 but does not change the mode of transmission from an excitatory (inhibitory) to an inhibitory (excitatory) communication. We speculate that such mechanism of presynaptic control might function in other systems 65 and be particularly effective in assigning the stimulus valence over a range of stimulus intensity.…”

Section: Discussioncontrasting

confidence: 99%

Presynaptic MAST Kinase Controls Bidirectional Post-Synaptic Responses to Convey Stimulus Valence in C. elegans

Nakano

Ikeda

Tsukada

et al. 2019

Preprint

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24Presynaptic plasticity is known to modulate the strength of synaptic transmission. 25However, it remains unknown whether regulation in presynaptic neurons alters the 26 directionality -positive or negative-of postsynaptic responses. We report here that the 27 C. elegans homologs of MAST kinase, Stomatin and Diacylglycerol kinase act in a 28 thermosensory neuron to elicit in its postsynaptic neuron an excitatory or inhibitory 29 response that correlates with the valence of thermal stimuli. By monitoring neural 30 activity of the valence-coding interneuron in freely behaving animals, we show that 31 the alteration between excitatory and inhibitory responses of the interneuron is 32 mediated by controlling the balance of two opposing signals released from the 33 presynaptic neuron. These alternative transmissions further generate opposing 34 behavioral outputs necessary for the navigation on thermal gradients. Our findings 35 reveal the previously unrecognized capability of presynaptic regulation to evoke 36 bidirectional postsynaptic responses and suggest a molecular mechanism of 37 determining stimulus valence. 38 4 neural circuit that promotes or inhibits feeding behaviors. 54Contrary to these developmentally programmed, stereotyped behaviors, the 55 valence associated with certain sensory stimuli can vary depending on the past experience, 56 the current environmental context and the stimulus intensity 9 . For example, olfactory 57 preferences to the same odorants can differ depending on the odorant concentration 10 . 58Studies of worms, flies and mammals suggested a common feature of neural mechanism 59 underlying the change in these odorant valences, wherein different concentrations of the 60 same odorants recruit distinct sets of olfactory neurons and consequently change the 61 perception of the same odorants [11][12][13] . However, the extent to which the brain utilizes 62 different encoding strategies for alternating stimulus valence remains largely unexplored. In 63 particular, the molecular and circuit mechanisms underlying the perception of altering 64 valence for other sensory modalities are not yet understood. 65The compact nervous system of C. elegans consisting of only 302 neurons 66 provides an excellent opportunity to explore these questions 14 . C. elegans exhibits 67 thermotaxis behavior 15 , in which the valence of thermal information varies depending on 68 5 the past experience, current temperature environment and feeding states. Specifically, the 69 temperature preference of C. elegans is plastic and determined by the cultivation 70 temperature, in which animals that are cultivated at a constant temperature with food 71 migrate toward that cultivation temperature on a thermal gradient without food 15 . When 72 animals were placed at the temperature below the cultivation temperature they migrate up 73 the thermal gradient, while above the cultivation temperature they move down the gradient, 74indicating that the valence associated with thermal stimuli alternates in opposing manners 75 dependin...

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Section: Discussioncontrasting

confidence: 99%

Presynaptic MAST Kinase Controls Bidirectional Post-Synaptic Responses to Convey Stimulus Valence in C. elegans

Nakano

Ikeda

Tsukada

et al. 2019

Preprint

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“…Although the expression of synaptic plasticity can be presynaptic, its induction depends on postsynaptic activity (Monday and Castillo, 2017). This implies the need for retrograde signals that communicate with the presynapse.…”

Section: Plasticity Of Probabilistic Synapsesmentioning

confidence: 99%

Computational roles of plastic probabilistic synapses

Montero

Sacramento

Costa

2019

Current Opinion in Neurobiology

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The probabilistic nature of synaptic transmission has remained enigmatic. However, recent developments have started to shed light on why the brain may rely on probabilistic synapses. Here, we start out by reviewing experimental evidence on the specificity and plasticity of synaptic response statistics. Next, we overview different computational perspectives on the function of plastic probabilistic synapses for constrained, statistical and deep learning. We highlight that all of these views require some form of optimisation of probabilistic synapses, which has recently gained support from theoretical analysis of long-term synaptic plasticity experiments. Finally, we contrast these different computational views and propose avenues for future research. Overall, we argue that the time is ripe for a better understanding of the computational functions of probabilistic synapses.

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“…Various forms of adaptive plasticity operate to adjust presynaptic release properties (Regehr, 2012;Kittel and Heckmann, 2016;Jackman and Regehr, 2017;Monday and Castillo, 2017;Van Vactor and Sigrist, 2017). PHP is a conserved mechanism for maintaining synaptic strength within a stable range (Cull-Candy et al, 1980;Frank, 2014;Davis and Muller, 2015).…”

Section: Distinct Regulation Of Cac-sfgfp Following the Chronic Exprementioning

confidence: 99%

Endogenous tagging reveals differential regulation of Ca²⁺channels at single AZs during presynaptic homeostatic potentiation and depression

Gratz

Goel

Bruckner

et al. 2017

Preprint

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Neurons communicate through Ca 2+ -dependent neurotransmitter release at presynaptic active zones (AZs). Neurotransmitter release properties play a key role in defining information flow in circuits and are tuned during multiple forms of plasticity. Despite their central role in determining neurotransmitter release properties, little is known about how Ca 2+ channel levels are modulated to calibrate synaptic function. We used CRISPR to tag the Drosophila CaV2 Ca 2+ channel Cacophony (Cac) and investigated the regulation of endogenous Ca 2+ channels during homeostatic plasticity in males in which all endogenous Cac channels are tagged. We found that heterogeneously distributed Cac is highly predictive of neurotransmitter release probability at individual AZs and differentially regulated during opposing forms of presynaptic homeostatic plasticity. Specifically, Cac levels at AZ are increased during chronic and acute presynaptic homeostatic potentiation (PHP), and live imaging during acute expression of PHP reveals proportional Ca 2+ channel accumulation across heterogeneous AZs. In contrast, endogenous Cac levels do not change during presynaptic homeostatic depression (PHD), implying that the reported reduction in Ca 2+ influx during PHD is achieved through functional adaptions to pre-existing Ca 2+ channels. Thus, distinct mechanisms bi-directionally modulate presynaptic Ca 2+ levels to maintain stable synaptic strength in response to diverse challenges, with Ca 2+ channel abundance providing a rapidly tunable substrate for potentiating neurotransmitter release over both acute and chronic timescales.

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Closing the gap: long-term presynaptic plasticity in brain function and disease

Cited by 50 publications

References 79 publications

Presynaptic MAST Kinase Controls Bidirectional Post-Synaptic Responses to Convey Stimulus Valence in C. elegans

Presynaptic MAST Kinase Controls Bidirectional Post-Synaptic Responses to Convey Stimulus Valence in C. elegans

Computational roles of plastic probabilistic synapses

Endogenous tagging reveals differential regulation of Ca²⁺channels at single AZs during presynaptic homeostatic potentiation and depression

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Closing the gap: long-term presynaptic plasticity in brain function and disease

Cited by 50 publications

References 79 publications

Presynaptic MAST Kinase Controls Bidirectional Post-Synaptic Responses to Convey Stimulus Valence in C. elegans

Presynaptic MAST Kinase Controls Bidirectional Post-Synaptic Responses to Convey Stimulus Valence in C. elegans

Computational roles of plastic probabilistic synapses

Endogenous tagging reveals differential regulation of Ca2+channels at single AZs during presynaptic homeostatic potentiation and depression

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Endogenous tagging reveals differential regulation of Ca²⁺channels at single AZs during presynaptic homeostatic potentiation and depression