Neuronal activity drives matching of pre- and postsynaptic function during synapse maturation

Kay, Louise; Humphreys, Lawrence; Eickholt, Britta J.; Burrone, Juan

doi:10.1038/nn.2826

Cited by 40 publications

(55 citation statements)

References 10 publications

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“…Furthermore, the correlation between the size of the activity-dependent pool and PSD-95 staining at individual synapses was significant at 14 DIV but not at 10 DIV. Previous data has shown matching of synaptic strength between presynaptic and postsynaptic compartments, both structurally (Schikorski and Stevens, 1999) and functionally (Tokuoka and Goda, 2008;Kay et al, 2011) in mature neurons. Previous data from our lab has demonstrated that, at 10 DIV, individual synapses show strong correlation at a structural level but no correlation functionally (Kay et al, 2011), begging the question: which side drives functional matching?…”

Section: Discussionmentioning

confidence: 88%

“…Previous data has shown matching of synaptic strength between presynaptic and postsynaptic compartments, both structurally (Schikorski and Stevens, 1999) and functionally (Tokuoka and Goda, 2008;Kay et al, 2011) in mature neurons. Previous data from our lab has demonstrated that, at 10 DIV, individual synapses show strong correlation at a structural level but no correlation functionally (Kay et al, 2011), begging the question: which side drives functional matching? Since we now show that a functional presynaptic readout fails to correlate with a structural postsynaptic readout at this developmental stage, it is likely that changes in presynaptic function are responsible for the emergence of a functional correlation.…”

Section: Discussionmentioning

confidence: 88%

See 1 more Smart Citation

Independent Vesicle Pools Underlie Different Modes of Release during Neuronal Development

Andreae

Fredj²,

Burrone³

2012

J. Neurosci.

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Mature presynaptic terminals release neurotransmitter both in response to activity and spontaneously. We found that axons of rat hippocampal neurons initially show very high levels of exclusively spontaneous release, which progressively switches over to the mature phenotype during synapse formation. These two modes of vesicle cycling derive from distinct pools throughout development and the initiation of activity-dependent release was independent of postsynaptic contacts, suggesting it is an autonomous presynaptic event.

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Section: Discussionmentioning

confidence: 88%

Section: Discussionmentioning

confidence: 88%

Independent Vesicle Pools Underlie Different Modes of Release during Neuronal Development

Andreae

Fredj²,

Burrone³

2012

J. Neurosci.

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“…This observation does not rule out the possibility that sensory feedback might modulate neuronal addition. A possible mechanism through which postsynaptic activity can influence neuronal addition is by activity-induced regulation of genes encoding molecules that promote survival of adult-born HVC neurons, axon path finding, and/or synapse formation (33,34). Interestingly, activity-induced guidance molecules are seasonally regulated in RA neurons of WCS; microarray analysis of cDNA extracted from RA revealed that the expression of guidance cue genes, including netrin 4 and galectin, is increased in breeding-condition birds (35).…”

Section: Discussionmentioning

confidence: 99%

Postsynaptic neural activity regulates neuronal addition in the adult avian song control system

Larson¹,

Wang²,

Gale

et al. 2013

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

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A striking feature of the nervous system is that it shows extensive plasticity of structure and function that allows animals to adjust to changes in their environment. Neural activity plays a key role in mediating experience-dependent neural plasticity and, thus, creates a link between the external environment, the nervous system, and behavior. One dramatic example of neural plasticity is ongoing neurogenesis in the adult brain. The role of neural activity in modulating neuronal addition, however, has not been well studied at the level of neural circuits. The avian song control system allows us to investigate how activity influences neuronal addition to a neural circuit that regulates song, a learned sensorimotor social behavior. In adult white-crowned sparrows, new neurons are added continually to the song nucleus HVC (proper name) and project their axons to its target nucleus, the robust nucleus of the arcopallium (RA). We report here that electrical activity in RA regulates neuronal addition to HVC. Decreasing neural activity in RA by intracerebral infusion of the GABA A receptor agonist muscimol decreased the number of new HVC neurons by 56%. Our results suggest that postsynaptic electrical activity influences the addition of new neurons into a functional neural circuit in adult birds. Songbirds provide a tractable model for understanding the mechanisms that regulate new neuron addition into functional circuits. Song is a learned sensorimotor behavior that is important for songbird reproduction. Song learning and production are regulated by a discrete, well-characterized neural circuit that includes HVC (proper name) and its target nucleus, the robust nucleus of the arcopallium (RA), both located in the avian forebrain (Fig. 1A) (2). In the adult Gambel's white-crowned sparrow (WCS), the song control system shows extreme seasonal neuroplasticity (reviewed in ref.3). Early in the breeding season, HVC and RA of WCS nearly double in volume. The increase in HVC volume results largely from an increase in new neuron incorporation, whereas the increase in RA volume results from increases in neuron size and spacing, but not number. RA neurons also show increased spontaneous electrical activity in the breeding season (4, 5). WCS typically produce only one song type that is longer and more stereotyped in structure during the breeding season (6, 7).HVC contains three types of neurons: HVC→RA and HVC→area X projection neurons and interneurons. During seasonal growth, most, if not all, neurons incorporated into HVC project to RA (ref. 8, but see ref. 9). Neural progenitor cells are born at the dorsal and ventral portion of the lateral ventricle and migrate from the ventricular zone (VZ) to HVC within 1 wk after birth (10). Over the next 2-3 wk, new neurons send axonal projections to RA (11). These new HVC→RA projection neurons are functional; they can fire action potentials in response to sound stimuli (12).Environment and experience play important roles in both brain development and adult neurogenesis. For example, duri...

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“…If this mechanism operates in vivo, it predicts an inverse relationship between P r and the summed synaptic strength onto a dendritic branch. In apparent conflict with this model, a positive correlation between P r and synaptic strength at cortical synapses has been reported (Hardingham et al 2010;Kay et al 2011), but because in these studies synaptic strength was measured at unitary connections, it remains an open possibility that such an inverse correlation exists at the level of summed dendritic input.…”

Section: Local and Quasi-local Forms Of Homeostatic Synaptic Plasticimentioning

confidence: 98%

Homeostatic Synaptic Plasticity: Local and Global Mechanisms for Stabilizing Neuronal Function

Turrigiano

2011

Cold Spring Harbor Perspectives in Biology

956

913

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Neural circuits must maintain stable function in the face of many plastic challenges, including changes in synapse number and strength, during learning and development. Recent work has shown that these destabilizing influences are counterbalanced by homeostatic plasticity mechanisms that act to stabilize neuronal and circuit activity. One such mechanism is synaptic scaling, which allows neurons to detect changes in their own firing rates through a set of calcium-dependent sensors that then regulate receptor trafficking to increase or decrease the accumulation of glutamate receptors at synaptic sites. Additional homeostatic mechanisms may allow local changes in synaptic activation to generate local synaptic adaptations, and network-wide changes in activity to generate network-wide adjustments in the balance between excitation and inhibition. The signaling pathways underlying these various forms of homeostatic plasticity are currently under intense scrutiny, and although dozens of molecular pathways have now been implicated in homeostatic plasticity, a clear picture of how homeostatic feedback is structured at the molecular level has not yet emerged. On a functional level, neuronal networks likely use this complex set of regulatory mechanisms to achieve homeostasis over a wide range of temporal and spatial scales.

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Neuronal activity drives matching of pre- and postsynaptic function during synapse maturation

Cited by 40 publications

References 10 publications

Independent Vesicle Pools Underlie Different Modes of Release during Neuronal Development

Independent Vesicle Pools Underlie Different Modes of Release during Neuronal Development

Postsynaptic neural activity regulates neuronal addition in the adult avian song control system

Homeostatic Synaptic Plasticity: Local and Global Mechanisms for Stabilizing Neuronal Function

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