Abstract
In the human neocortex coherent interlaminar theta oscillations are driven by deep cortical layers, suggesting neurons in these layers exhibit distinct electrophysiological properties. To characterize this potential distinctiveness, we use in vitro whole-cell recordings from cortical layers 2 and 3 (L2&3), layer 3c (L3c) and layer 5 (L5) of the human cortex. Across all layers we observe notable heterogeneity, indicating human cortical pyramidal neurons are an electrophysiologically diverse population. L5 pyramidal cells are the most excitable of these neurons and exhibit the most prominent sag current (abolished by blockade of the hyperpolarization activated cation current, Ih). While subthreshold resonance is more common in L3c and L5, we rarely observe this resonance at frequencies greater than 2 Hz. However, the frequency dependent gain of L5 neurons reveals they are most adept at tracking both delta and theta frequency inputs, a unique feature that may indirectly be important for the generation of cortical theta oscillations.
Highlights
In the human neocortex coherent interlaminar theta oscillations are driven by deep cortical layers, suggesting neurons in these layers exhibit distinct electrophysiological properties
Whole-cell patch clamp recordings were obtained from human neocortical neurons located in layers 2 and 3 (L2&3), layer 3c (L3c), and layer 5 (L5) within acute brain slices collected from 61 patients
Considering each broad cortical layer as a group, we found that there is a gradient of increased excitability from superficial to deeper layer pyramidal cells, with L2&3 pyramidal cells demonstrating more hyperpolarized resting potentials, lower input resistances and larger rheobase required for spike generation, enhanced spike frequency adaptation, and steeper and larger amplitude STAs
Summary
In the human neocortex coherent interlaminar theta oscillations are driven by deep cortical layers, suggesting neurons in these layers exhibit distinct electrophysiological properties. As we explore what is uniquely human about the human brain in order to, for example, tackle the increasing societal burden of neurological and neuropsychiatric conditions[15,16], infusing computational models with human derived microscopic and mesoscopic cellular and circuit properties will be critically important. In this context, our previous experiments in human cortical slices have demonstrated that spontaneous theta-like activity, the most ubiquitous oscillation in the human brain[17], can be induced by application of cholinergic and glutamatergic agonists[9]. Given the role of intrinsic electrophysiological properties in the generation of oscillations[13] and the finding that deep layer theta leads superficial layer theta in phase, we reasoned that deep layer neurons in the human neocortex are likely endowed with distinct biophysical properties that enable them to “drive” such interlaminar activity
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