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Kole, K.

Publications and source records attributed to Kole, K..

8 recordsLinked to original sources

Neuromodulatory Control of Cortical Function: Cell-Type Specific Regulation of Neuronal Information Transfer

Neuromodulatory systems such as dopamine and acetylcholine enable cortical circuits to rapidly shift between behavioral states, yet it remains unclear how receptor-specific signaling reshapes what single neurons compute. Here we combined whole-cell recordings from excitatory and inhibitory neurons in layer 2/3 of mouse somatosensory cortex with information-theoretic analyses under frozen-noise stimulation. We quantified stimulus-to-spike information transfer and profiled each neuron across four functional domains: passive membrane biophysics, action potential dynamics, intrinsic adaptation currents, and input feature selectivity captured by spike-triggered averages. Activation of D1, D2, or M1 receptors produced cell-type and receptor-specific changes in fractional information and firing output, demonstrating that neuromodulators regulate encoding beyond simple gain control. Unsupervised clustering revealed that receptor activation reshapes neuronal functional identities, consistent with a dynamic computational phenotype. To identify the organizing principle underlying these transitions, we applied multi-set correlation and factor analysis and found that neuromodulation systematically reorganizes covariance among functional domains. In excitatory neurons, dopaminergic activation led to a decreased coordination between input feature selectivity and other functional properties while strengthening coordination among response based features such as spike dynamics and adaptation. Inhibitory neurons, by contrast, generally exhibited increased coordination across domains. These findings identify neuromodulation as a reconfiguration signal that reshapes not only individual cellular properties but also the architecture linking them, thereby dynamically expanding the computational repertoire of cortical circuits.

neuroscience↗

Robust activity-dependent mitochondrial calcium dynamics at the AIS is dispensable for action potential generation

Mitochondria are diverse and multifaceted intracellular organelles regulating oxidative energy supply, lipid metabolism and calcium (Ca2+) signaling. In neurons the spatial sequestration of cytoplasmic Ca2+ by mitochondria plays a critical role in determining activity-dependent spine plasticity, shaping the presynaptic transmitter release characteristics and contributing to sustained action potential firing. Here, we tested the hypothesis that mitochondria at the axon initial segment (AIS) affect the microdomain cytoplasmic Ca2+ transients, thereby regulating Ca2+-dependent voltage-gated ion channels at the plasma membrane and initiation of action potentials. Using 3D electron microscopy (EM) reconstructions and virally injecting genetically encoded fluorescence indicators we visualized the ultrastructure and distribution of mitochondria selectively in thick-tufted layer 5 pyramidal neurons. We found that most mitochondria were stably clustered to the proximal AIS, while few were observed at distal sites. Simultaneous two-photon imaging of action potential-dependent cytoplasmic and mitochondrial Ca2+, combined with electrophysiological recordings showed the AIS mitochondria exhibit powerful activity-dependent cytosolic Ca2+ uptake. However, while intracellular application of the mitochondrial Ca2+ uniporter inhibitor Ru360 fully blocked mitochondrial Ca2+ import, it did not affect action potential input-output function, action potential dynamics nor the ability to produce high-frequency burst output. Together, the results indicate that AIS mitochondria are dispensable for temporal and rate encoding, suggesting that mt-Ca2+ buffering at the AIS may be involved in non-electrical roles, including AIS maintenance or axonal transport.

neuroscience↗

Myelination-dependent mitochondria clustering and calcium buffering in parvalbumin interneuron axons

Parvalbumin-expressing (PV+) basket cells are fast-spiking interneurons that exert critical control over local neuronal circuit activity and oscillations. PV+ interneuron axons are partially myelinated but the electrical and metabolic roles of myelin in axonal functions remain poorly understood. Here, we developed Cre-dependent AAV vectors for cell type-specific investigation of mitochondria with genetically encoded fluorescent probes. Single-cell reconstructions and mining of ultrastructural data revealed that mitochondria selectively cluster to myelinated segments of PV+ basket cell axons. Cuprizone-induced demyelination abolished mitochondrial clustering in PV+ axons but increased axonal mitochondrial densities in excitatory axons. The internodal clustering of mitochondria was preserved with genetic deletion of myelin basic protein, suggesting that noncompacted myelin is sufficient. Finally, two-photon imaging of action potential-evoked mitochondrial calcium (mt-Ca2+) responses showed that internodal mitochondria did not contribute in buffering activity-dependent Ca2+ influx. These findings suggest that oligodendrocyte-PV+ axon signaling assembles mitochondria to branch selectively fine-tune metabolic demands.

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A whole-cell recording database of neuromodulatory action in the adult neocortex

BackgroundThe recent release of two large intracellular electrophysiological databases now allows high-dimensional systematic analysis of mechanisms of information processing in the neocortex. Here, to complement these efforts, we introduce a freely and publicly available database that provides a comparative insight into the role of various neuromodulatory transmitters in controlling neural information processing. FindingsA database of in vitro whole-cell patch-clamp recordings from primary somatosensory and motor cortices (layers 2/3) of the adult mice (2-15 months old) from both sexes is introduced. A total of 464 current-clamp experiments from identified excitatory and inhibitory neurons are provided. Experiments include recordings with (i) Step-and-Hold protocol during which the current was transiently held at 10 steps, gradually increasing in amplitude, (ii) "Frozen Noise" injections that model the amplitude and time-varying nature of synaptic inputs to a neuron in biological networks. All experiments follow a within neuron across drug design which includes a vehicle control and a modulation of one of the following targets in the same neuron: dopamine and its receptors D1R, D2R, serotonin 5HT1f receptor, norepinephrine Alpha1, and acetylcholine M1 receptors. ConclusionsThis dataset is the first to provide a systematic and comparative insight into the role of the selected neuromodulators in controlling cellular excitability. The data will help to mechanistically address how bottom-up information processing can be modulated, providing a reference for studying neural coding characteristics and revealing the contribution of neuromodulation to information processing.

neuroscience↗

Assessing the utility of MAGNETO to control neuronal excitability in the somatosensory cortex

Magnetic neuromodulation has outstanding promise for the development of novel neural interfaces without direct physical intervention with the brain. Here we tested the utility of Magneto in the adult somatosensory cortex by performing whole-cell intracellular recordings in vitro and extracellular recordings in freely moving mice. Results show that magnetic stimulation does not alter subthreshold membrane excitability or contribute to the generation of action potentials in virally transduced neurons expressing Magneto.

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A databank for intracellular electrophysiological mapping of the adult somatosensory cortex

BackgroundNeurons in the supragranular layers of the somatosensory cortex integrate sensory (bottom-up) and cognitive/perceptual (top-down) information as they orchestrate communication across cortical columns. It has been inferred, based on intracellular recordings from juvenile animals, that supragranular neurons are electrically mature by the fourth postnatal week. However, the dynamics of the neuronal integration in the adulthood is largely unknown. Electrophysiological characterization of the active properties of these neurons throughout adulthood will help to address the biophysical and computational principles of the neuronal integration.\n\nFindingsHere we provide a database of whole-cell intracellular recordings from 315 neurons located in the supragranular layers (L2/3) of the primary somatosensory cortex in adult mice (9-45 weeks old) from both sexes (females, N=195; males, N=120). Data include 361 somatic current-clamp (CC) and 476 voltage-clamp (VC) experiments, recorded using a step-and-hold protocol (CC, N=257; VC, N=46), frozen noise injections (CC, N=104) and triangular voltage sweeps (VC, 10 (N=132), 50 (N=146) and 100 ms (N=152)), from regular spiking (N=169) and fast-spiking neurons (N=66).\n\nConclusionsThe data can be used to systematically study the properties of somatic integration, and the principles of action potential generation across sexes and across electrically characterized neuronal classes in adulthood. Understanding the principles of the somatic transformation of postsynaptic potentials into action potentials will shed light onto the computational principles of intracellular information transfer in single neurons and information processing in neuronal networks, helping to recreate neuronal functions in artificial systems.

neuroscience↗

Molecules of map plasticity in the somatosensory cortex

Sensory maps are representations of the sensory epithelia in the brain. Despite the intuitive explanatory power behind sensory maps as being neuronal precursors to sensory perception, and sensory cortical plasticity as a neural correlate of perceptual learning, molecular mechanisms that regulate map plasticity are not well understood. Here we perform a meta-analysis of transcriptional and translational changes during altered whisker use to nominate the major molecular correlates of experience-dependent map plasticity in the barrel cortex. We argue that brain plasticity is a systems level response, involving all cell classes, from neuron and glia to non-neuronal cells including endothelia. Using molecular pathway analysis, we further propose a gene regulatory network that could couple activity dependent changes in neurons to adaptive changes in neurovasculature, and finally we show that transcriptional regulations observed in major brain disorders target genes that are modulated by altered sensory experience. Thus understanding the molecular mechanisms of experience-dependent plasticity of sensory maps might help to unravel the cellular events that shape brain plasticity in health and disease.\n\nHighlightsO_LIExperience alters gene transcription in all major cell types of the brain\nC_LIO_LIGene expression profile during brain plasticity is cell-type specific\nC_LIO_LITemporal profile of gene expression is dynamic, regulated by recent experience\nC_LIO_LINeural activity-dependent gene regulation might cause neurovascular reorganization\nC_LIO_LIGenes that are regulated by experience are commonly dysregulated in brain disorders\nC_LI

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Neocortical microdissection at columnar and laminar resolution for molecular interrogation

The heterogeneous organization of the mammalian neocortex poses a challenge to elucidate the molecular mechanisms underlying its physiological processes. Although high-throughput molecular methods are increasingly deployed in neuroscience, their anatomical specificity is often lacking. Here we introduce a targeted microdissection technique that enables extraction of high-quality RNA and proteins at high anatomical resolution from acutely prepared brain slices. We exemplify its utility by isolating single cortical columns and laminae from the mouse primary somatosensory (barrel) cortex. Tissues can be isolated from living slices in minutes, and the extracted RNA and protein are of sufficient quantity and quality to be used for RNA-sequencing and mass spectrometry. This technique will help to increase the anatomical specificity of molecular studies of the neocortex, and the brain in general as it is applicable to any brain structure that can be identified using optical landmarks in living slices.

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