High-fidelity dendritic sodium spike generation in human layer 2/3 neocortical pyramidal neurons

Gooch, Helen; Bluett, Tobias; Perumal, Madhusoothanan B.; Vo, Hong D.; Fletcher, Lee N.; Papacostas, Jason; Jeffree, Rosalind L.; Wood, Martin; Colditz, Michael; McMillen, Jason; Tsahtsarlis, Tony; Amato, Damian; Campbell, Robert F.; Gillinder, Lisa; Williams, Stephen R.

doi:10.1016/j.celrep.2022.111500

Cited by 12 publications

(14 citation statements)

References 55 publications

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“…Recent experiments indicated that the C m of human L2/3 PCs might be significantly lower compared to rodents 25 and modeling studies suggested that the decrease in C m could lead to increased conduction speed and fewer synapses being able to evoke suprathreshold events in human PCs 25 . However, a separate line of experiments could not detect differences in the C m of L5 PCs between humans and rodents 7 , or L2/3 PCs 26 thus, to test whether C m is a component in producing elevated signal propagation velocity in human dendrites, we directly measured the C m values of human and rat PCs by pulling nucleated patches 25 (Fig. 4A,B).…”

Section: Resultsmentioning

confidence: 99%

Accelerated signal propagation speed in human neocortical dendrites

Oláh

Lákovics

Shapira

et al. 2022

Preprint

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Human-specific cognitive abilities depend on information processing in the cerebral cortex, where neurons are significantly larger and sparser compared to rodents. We found that, in synaptically-connected layer 2/3 pyramidal cells (L2/3 PCs), soma-to-soma signal propagation delay is similar in humans and rodents. Thus, to compensate for the increase in neurons size, membrane potential changes must propagate faster in human axons and/or dendrites. Dual somato-dendritic and somato-axonal patch recordings show that action potentials (APs) propagation speed is similar in human and rat axons, but the forward propagation of the EPSPs and the back-propagating APs are ~1.7-fold faster in human dendrites. Faithful biophysical models of human and rat L2/3 PCs, combined with pharmacological manipulations of membrane properties, showed that the larger dendritic diameter, combined with differences in cable properties, underlie the accelerated signal propagation in human cortical circuits. The implication for information processing in the human brain are discussed.

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Section: Resultsmentioning

confidence: 99%

Accelerated signal propagation speed in human neocortical dendrites

Oláh

Lákovics

Shapira

et al. 2022

Preprint

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“…However, their in vivo recording of rat hippocampus exhibited no correlation of CA1 spindle phase with spiking in principal cells or interneurons, similar to the absence of correlation that we observed and their lack of co-modulation in human intracranial depth electrodes 6 . Active ion channels in axons separate from those that propagate spikes may be similar to the active calcium channels in dendrites 27 . Our failure to find consistent loss of slow wave amplitude with distance along the axon suggests that slow wave-spindle wave oscillations are not passive electrotonic conductances originating in their somata or dendrites.…”

Section: Discussionmentioning

confidence: 99%

Spindle oscillations in communicating axons within a reconstituted hippocampal formation are strongest in CA3 without thalamus

Wang,

Lassers,

Vakilna

et al. 2024

Sci Rep

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Spindle-shaped waves of oscillations emerge in EEG scalp recordings during human and rodent non-REM sleep. The association of these 10–16 Hz oscillations with events during prior wakefulness suggests a role in memory consolidation. Human and rodent depth electrodes in the brain record strong spindles throughout the cortex and hippocampus, with possible origins in the thalamus. However, the source and targets of the spindle oscillations from the hippocampus are unclear. Here, we employed an in vitro reconstruction of four subregions of the hippocampal formation with separate microfluidic tunnels for single axon communication between subregions assembled on top of a microelectrode array. We recorded spontaneous 400–1000 ms long spindle waves at 10–16 Hz in single axons passing between subregions as well as from individual neurons in those subregions. Spindles were nested within slow waves. The highest amplitudes and most frequent occurrence suggest origins in CA3 neurons that send feed-forward axons into CA1 and feedback axons into DG. Spindles had 50–70% slower conduction velocities than spikes and were not phase-locked to spikes suggesting that spindle mechanisms are independent of action potentials. Therefore, consolidation of declarative-cognitive memories in the hippocampus may be separate from the more easily accessible consolidation of memories related to thalamic motor function.

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“…Interestingly, human pyramidal neurons have been shown to have greater dendritic compartmentalization than the more commonly studied rodent cortical neurons [70]. In combination with their larger dendritic arbours [71], distinct biophysical composition [72] and highly plastic neurons [73][74][75], this may provide human neurons with enhanced computational abilities and specific dendritic integrative properties [76][77][78]. Taken together, signalling within individual dendritic branches is plastic in vivo, which may serve to enhance specific input streams and increase the computational capabilities of a single pyramidal neuron.…”

Section: Dendritic Branch Plasticity In Vivomentioning

confidence: 99%

The plasticity of pyramidal neurons in the behaving brain

Regele-Blasco,

Palmer

2024

Phil. Trans. R. Soc. B

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Neurons are plastic. That is, they change their activity according to different behavioural conditions. This endows pyramidal neurons with an incredible computational power for the integration and processing of synaptic inputs. Plasticity can be investigated at different levels of investigation within a single neuron, from spines to dendrites, to synaptic input. Although most of our knowledge stems from the in vitro brain slice preparation, plasticity plays a vital role during behaviour by providing a flexible substrate for the execution of appropriate actions in our ever-changing environment. Owing to advances in recording techniques, the plasticity of neurons and the neural networks in which they are embedded is now beginning to be realized in the in vivo intact brain. This review focuses on the structural and functional synaptic plasticity of pyramidal neurons , with a specific focus on the latest developments from in vivo studies. This article is part of a discussion meeting issue ‘Long-term potentiation: 50 years on'.

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High-fidelity dendritic sodium spike generation in human layer 2/3 neocortical pyramidal neurons

Cited by 12 publications

References 55 publications

Accelerated signal propagation speed in human neocortical dendrites

Accelerated signal propagation speed in human neocortical dendrites

Spindle oscillations in communicating axons within a reconstituted hippocampal formation are strongest in CA3 without thalamus

The plasticity of pyramidal neurons in the behaving brain

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