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Naturalistic stimulation drives opposing heterosynaptic plasticity at two inputs to songbird cortex.

ABSTRACT: Songbirds learn precisely sequenced motor skills (songs) subserved by distinct brain areas, including the premotor cortical analog HVC, which is essential for producing learned song, and a 'cortical'-basal ganglia loop required for song plasticity. Inputs from these nuclei converge in RA (robust nucleus of the arcopallium), making it a likely locus for song learning. However, activity-dependent synaptic plasticity has never been described in either input. Using a slice preparation, we found that stimulation patterns based on singing-related activity were able to drive opposing changes in the strength of RA's inputs: when one input was potentiated, the other was depressed, with the direction and magnitude of changes depending on the relative timing of stimulation of the inputs. Moreover, pharmacological manipulations that blocked synaptic plasticity in vitro also prevented reinforcement-driven changes to song in vivo. Together, these findings highlight the importance of precise timing in the basal ganglia-motor cortical interactions subserving adaptive motor skills.

SUBMITTER: Mehaffey WH

PROVIDER: S-EPMC5726397 | biostudies-literature | 2015 Sep

REPOSITORIES: biostudies-literature

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Naturalistic stimulation drives opposing heterosynaptic plasticity at two inputs to songbird cortex.

Mehaffey W Hamish WH Doupe Allison J AJ

Nature neuroscience 20150803 9

Songbirds learn precisely sequenced motor skills (songs) subserved by distinct brain areas, including the premotor cortical analog HVC, which is essential for producing learned song, and a 'cortical'-basal ganglia loop required for song plasticity. Inputs from these nuclei converge in RA (robust nucleus of the arcopallium), making it a likely locus for song learning. However, activity-dependent synaptic plasticity has never been described in either input. Using a slice preparation, we found that ...[more]

PMID: 26237364

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Project description:AbstractIn biology, heterosynaptic plasticity maintains homeostasis in synaptic inputs during associative learning and memory, and initiates long-term changes in synaptic strengths that nonspecifically modulate different synapse types. In bioinspired neuromorphic circuits, heterosynaptic plasticity may be used to extend the functionality of two-terminal, biomimetic memristors. In this article, we explore how changes in the pH of droplet interface bilayer aqueous solutions modulate the memristive responses of a lipid bilayer membrane in the pH range 4.97-7.40. Surprisingly, we did not find conclusive evidence for pH-dependent shifts in the voltage thresholds (V*) needed for alamethicin ion channel formation in the membrane. However, we did observe a clear modulation in the dynamics of pore formation with pH in time-dependent, pulsed voltage experiments. Moreover, at the same voltage, lowering the pH resulted in higher steady-state currents because of increased numbers of conductive peptide ion channels in the membrane. This was due to increased partitioning of alamethicin monomers into the membrane at pH 4.97, which is below the pKa (~5.3-5.7) of carboxylate groups on the glutamate residues of the peptide, making the monomers more hydrophobic. Neutralization of the negative charges on these residues, under acidic conditions, increased the concentration of peptide monomers in the membrane, shifting the equilibrium concentrations of peptide aggregate assemblies in the membrane to favor greater numbers of larger, increasingly more conductive pores. It also increased the relaxation time constants for pore formation and decay, and enhanced short-term facilitation and depression of the switching characteristics of the device. Modulating these thresholds globally and independently of alamethicin concentration and applied voltage will enable the assembly of neuromorphic computational circuitry with enhanced functionality.Impact statementWe describe how to use pH as a modulatory "interneuron" that changes the voltage-dependent memristance of alamethicin ion channels in lipid bilayers by changing the structure and dynamical properties of the bilayer. Having the ability to independently control the threshold levels for pore conduction from voltage or ion channel concentration enables additional levels of programmability in a neuromorphic system. In this article, we note that barriers to conduction from membrane-bound ion channels can be lowered by reducing solution pH, resulting in higher currents, and enhanced short-term learning behavior in the form of paired-pulse facilitation. Tuning threshold values with environmental variables, such as pH, provide additional training and learning algorithms that can be used to elicit complex functionality within spiking neural networks.Graphical abstractSupplementary informationThe online version contains supplementary material available at 10.1557/s43577-022-00344-z.

Dataset Information

Naturalistic stimulation drives opposing heterosynaptic plasticity at two inputs to songbird cortex.

Publications

Naturalistic stimulation drives opposing heterosynaptic plasticity at two inputs to songbird cortex.

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